diff --git a/.changelog/14796.txt b/.changelog/14796.txt
new file mode 100644
index 0000000000..d39552c857
--- /dev/null
+++ b/.changelog/14796.txt
@@ -0,0 +1,3 @@
+```release-note:improvement
+peering: require TLS for peering connections using server cert signed by Connect CA
+```
diff --git a/agent/agent_endpoint_test.go b/agent/agent_endpoint_test.go
index ac4807edd6..6e52157dfe 100644
--- a/agent/agent_endpoint_test.go
+++ b/agent/agent_endpoint_test.go
@@ -1443,8 +1443,8 @@ func TestAgent_Self(t *testing.T) {
 			}
 			ports = {
 				grpc = -1
-			}
-			`,
+				grpc_tls = -1
+			}`,
 			expectXDS: false,
 			grpcTLS:   false,
 		},
@@ -1453,7 +1453,9 @@ func TestAgent_Self(t *testing.T) {
 			node_meta {
 				somekey = "somevalue"
 			}
-			`,
+			ports = {
+				grpc_tls = -1
+			}`,
 			expectXDS: true,
 			grpcTLS:   false,
 		},
@@ -1461,8 +1463,7 @@ func TestAgent_Self(t *testing.T) {
 			hcl: `
 				node_meta {
 					somekey = "somevalue"
-				}
-				`,
+				}`,
 			expectXDS: true,
 			grpcTLS:   true,
 		},
diff --git a/agent/connect/testing_ca.go b/agent/connect/testing_ca.go
index 343de77bc4..06d965ce6e 100644
--- a/agent/connect/testing_ca.go
+++ b/agent/connect/testing_ca.go
@@ -183,8 +183,7 @@ func TestCAWithKeyType(t testing.T, xc *structs.CARoot, keyType string, keyBits
 	return testCA(t, xc, keyType, keyBits, 0)
 }
 
-func testLeafWithID(t testing.T, spiffeId CertURI, root *structs.CARoot, keyType string, keyBits int, expiration time.Duration) (string, string, error) {
-
+func testLeafWithID(t testing.T, spiffeId CertURI, dnsSAN string, root *structs.CARoot, keyType string, keyBits int, expiration time.Duration) (string, string, error) {
 	if expiration == 0 {
 		// this is 10 years
 		expiration = 10 * 365 * 24 * time.Hour
@@ -238,6 +237,7 @@ func testLeafWithID(t testing.T, spiffeId CertURI, root *structs.CARoot, keyType
 		NotBefore:      time.Now(),
 		AuthorityKeyId: testKeyID(t, caSigner.Public()),
 		SubjectKeyId:   testKeyID(t, pkSigner.Public()),
+		DNSNames:       []string{dnsSAN},
 	}
 
 	// Create the certificate, PEM encode it and return that value.
@@ -263,7 +263,7 @@ func TestAgentLeaf(t testing.T, node string, datacenter string, root *structs.CA
 		Agent:      node,
 	}
 
-	return testLeafWithID(t, spiffeId, root, DefaultPrivateKeyType, DefaultPrivateKeyBits, expiration)
+	return testLeafWithID(t, spiffeId, "", root, DefaultPrivateKeyType, DefaultPrivateKeyBits, expiration)
 }
 
 func testLeaf(t testing.T, service string, namespace string, root *structs.CARoot, keyType string, keyBits int) (string, string, error) {
@@ -275,7 +275,7 @@ func testLeaf(t testing.T, service string, namespace string, root *structs.CARoo
 		Service:    service,
 	}
 
-	return testLeafWithID(t, spiffeId, root, keyType, keyBits, 0)
+	return testLeafWithID(t, spiffeId, "", root, keyType, keyBits, 0)
 }
 
 // TestLeaf returns a valid leaf certificate and it's private key for the named
@@ -305,7 +305,23 @@ func TestMeshGatewayLeaf(t testing.T, partition string, root *structs.CARoot) (s
 		Datacenter: "dc1",
 	}
 
-	certPEM, keyPEM, err := testLeafWithID(t, spiffeId, root, DefaultPrivateKeyType, DefaultPrivateKeyBits, 0)
+	certPEM, keyPEM, err := testLeafWithID(t, spiffeId, "", root, DefaultPrivateKeyType, DefaultPrivateKeyBits, 0)
+	if err != nil {
+		t.Fatalf(err.Error())
+	}
+	return certPEM, keyPEM
+}
+
+func TestServerLeaf(t testing.T, dc string, root *structs.CARoot) (string, string) {
+	t.Helper()
+
+	spiffeID := &SpiffeIDServer{
+		Datacenter: dc,
+		Host:       fmt.Sprintf("%s.consul", TestClusterID),
+	}
+	san := PeeringServerSAN(dc, TestTrustDomain)
+
+	certPEM, keyPEM, err := testLeafWithID(t, spiffeID, san, root, DefaultPrivateKeyType, DefaultPrivateKeyBits, 0)
 	if err != nil {
 		t.Fatalf(err.Error())
 	}
diff --git a/agent/consul/leader_peering_test.go b/agent/consul/leader_peering_test.go
index 7df1a4b065..43e7b533db 100644
--- a/agent/consul/leader_peering_test.go
+++ b/agent/consul/leader_peering_test.go
@@ -22,6 +22,7 @@ import (
 	"google.golang.org/protobuf/proto"
 
 	"github.com/hashicorp/consul/acl"
+	"github.com/hashicorp/consul/agent/connect"
 	"github.com/hashicorp/consul/agent/consul/state"
 	"github.com/hashicorp/consul/agent/structs"
 	"github.com/hashicorp/consul/api"
@@ -34,27 +35,23 @@ import (
 )
 
 func TestLeader_PeeringSync_Lifecycle_ClientDeletion(t *testing.T) {
-	t.Run("without-tls", func(t *testing.T) {
-		testLeader_PeeringSync_Lifecycle_ClientDeletion(t, false)
-	})
-	t.Run("with-tls", func(t *testing.T) {
-		testLeader_PeeringSync_Lifecycle_ClientDeletion(t, true)
-	})
-}
-
-func testLeader_PeeringSync_Lifecycle_ClientDeletion(t *testing.T, enableTLS bool) {
 	if testing.Short() {
 		t.Skip("too slow for testing.Short")
 	}
 
+	ca := connect.TestCA(t, nil)
 	_, acceptor := testServerWithConfig(t, func(c *Config) {
 		c.NodeName = "acceptor"
 		c.Datacenter = "dc1"
 		c.TLSConfig.Domain = "consul"
-		if enableTLS {
-			c.TLSConfig.GRPC.CAFile = "../../test/hostname/CertAuth.crt"
-			c.TLSConfig.GRPC.CertFile = "../../test/hostname/Bob.crt"
-			c.TLSConfig.GRPC.KeyFile = "../../test/hostname/Bob.key"
+		c.GRPCTLSPort = freeport.GetOne(t)
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
 		}
 	})
 	testrpc.WaitForLeader(t, acceptor.RPC, "dc1")
@@ -94,11 +91,6 @@ func testLeader_PeeringSync_Lifecycle_ClientDeletion(t *testing.T, enableTLS boo
 		c.NodeName = "dialer"
 		c.Datacenter = "dc2"
 		c.PrimaryDatacenter = "dc2"
-		if enableTLS {
-			c.TLSConfig.GRPC.CAFile = "../../test/hostname/CertAuth.crt"
-			c.TLSConfig.GRPC.CertFile = "../../test/hostname/Betty.crt"
-			c.TLSConfig.GRPC.KeyFile = "../../test/hostname/Betty.key"
-		}
 	})
 	testrpc.WaitForLeader(t, dialer.RPC, "dc2")
 
@@ -169,13 +161,22 @@ func TestLeader_PeeringSync_Lifecycle_UnexportWhileDown(t *testing.T) {
 	}
 
 	// Reserve a gRPC port so we can restart the accepting server with the same port.
-	ports := freeport.GetN(t, 1)
-	dialingServerPort := ports[0]
+	dialingServerPort := freeport.GetOne(t)
 
+	ca := connect.TestCA(t, nil)
 	_, acceptor := testServerWithConfig(t, func(c *Config) {
 		c.NodeName = "acceptor"
 		c.Datacenter = "dc1"
 		c.TLSConfig.Domain = "consul"
+		c.GRPCTLSPort = freeport.GetOne(t)
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
+		}
 	})
 	testrpc.WaitForLeader(t, acceptor.RPC, "dc1")
 
@@ -207,10 +208,11 @@ func TestLeader_PeeringSync_Lifecycle_UnexportWhileDown(t *testing.T) {
 	// Bring up dialer and establish a peering with acceptor's token so that it attempts to dial.
 	_, dialer := testServerWithConfig(t, func(c *Config) {
 		c.NodeName = "dialer"
-		c.Datacenter = "dc1"
+		c.Datacenter = "dc2"
+		c.PrimaryDatacenter = "dc2"
 		c.GRPCPort = dialingServerPort
 	})
-	testrpc.WaitForLeader(t, dialer.RPC, "dc1")
+	testrpc.WaitForLeader(t, dialer.RPC, "dc2")
 
 	// Create a peering at dialer by establishing a peering with acceptor's token
 	ctx, cancel = context.WithTimeout(context.Background(), 3*time.Second)
@@ -344,27 +346,23 @@ func TestLeader_PeeringSync_Lifecycle_UnexportWhileDown(t *testing.T) {
 }
 
 func TestLeader_PeeringSync_Lifecycle_ServerDeletion(t *testing.T) {
-	t.Run("without-tls", func(t *testing.T) {
-		testLeader_PeeringSync_Lifecycle_AcceptorDeletion(t, false)
-	})
-	t.Run("with-tls", func(t *testing.T) {
-		testLeader_PeeringSync_Lifecycle_AcceptorDeletion(t, true)
-	})
-}
-
-func testLeader_PeeringSync_Lifecycle_AcceptorDeletion(t *testing.T, enableTLS bool) {
 	if testing.Short() {
 		t.Skip("too slow for testing.Short")
 	}
 
+	ca := connect.TestCA(t, nil)
 	_, acceptor := testServerWithConfig(t, func(c *Config) {
 		c.NodeName = "acceptor"
 		c.Datacenter = "dc1"
 		c.TLSConfig.Domain = "consul"
-		if enableTLS {
-			c.TLSConfig.GRPC.CAFile = "../../test/hostname/CertAuth.crt"
-			c.TLSConfig.GRPC.CertFile = "../../test/hostname/Bob.crt"
-			c.TLSConfig.GRPC.KeyFile = "../../test/hostname/Bob.key"
+		c.GRPCTLSPort = freeport.GetOne(t)
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
 		}
 	})
 	testrpc.WaitForLeader(t, acceptor.RPC, "dc1")
@@ -399,11 +397,6 @@ func testLeader_PeeringSync_Lifecycle_AcceptorDeletion(t *testing.T, enableTLS b
 		c.NodeName = "dialer"
 		c.Datacenter = "dc2"
 		c.PrimaryDatacenter = "dc2"
-		if enableTLS {
-			c.TLSConfig.GRPC.CAFile = "../../test/hostname/CertAuth.crt"
-			c.TLSConfig.GRPC.CertFile = "../../test/hostname/Betty.crt"
-			c.TLSConfig.GRPC.KeyFile = "../../test/hostname/Betty.key"
-		}
 	})
 	testrpc.WaitForLeader(t, dialer.RPC, "dc2")
 
@@ -476,7 +469,7 @@ func TestLeader_PeeringSync_FailsForTLSError(t *testing.T) {
 	t.Run("server-name-validation", func(t *testing.T) {
 		testLeader_PeeringSync_failsForTLSError(t, func(token *structs.PeeringToken) {
 			token.ServerName = "wrong.name"
-		}, `transport: authentication handshake failed: x509: certificate is valid for server.dc1.consul, bob.server.dc1.consul, not wrong.name`)
+		}, `transport: authentication handshake failed: x509: certificate is valid for server.dc1.peering.11111111-2222-3333-4444-555555555555.consul, not wrong.name`)
 	})
 	t.Run("bad-ca-roots", func(t *testing.T) {
 		wrongRoot, err := ioutil.ReadFile("../../test/client_certs/rootca.crt")
@@ -491,14 +484,20 @@ func TestLeader_PeeringSync_FailsForTLSError(t *testing.T) {
 func testLeader_PeeringSync_failsForTLSError(t *testing.T, tokenMutateFn func(token *structs.PeeringToken), expectErr string) {
 	require.NotNil(t, tokenMutateFn)
 
+	ca := connect.TestCA(t, nil)
 	_, s1 := testServerWithConfig(t, func(c *Config) {
 		c.NodeName = "bob"
 		c.Datacenter = "dc1"
 		c.TLSConfig.Domain = "consul"
-
-		c.TLSConfig.GRPC.CAFile = "../../test/hostname/CertAuth.crt"
-		c.TLSConfig.GRPC.CertFile = "../../test/hostname/Bob.crt"
-		c.TLSConfig.GRPC.KeyFile = "../../test/hostname/Bob.key"
+		c.GRPCTLSPort = freeport.GetOne(t)
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
+		}
 	})
 	testrpc.WaitForLeader(t, s1.RPC, "dc1")
 
@@ -541,10 +540,6 @@ func testLeader_PeeringSync_failsForTLSError(t *testing.T, tokenMutateFn func(to
 		c.NodeName = "betty"
 		c.Datacenter = "dc2"
 		c.PrimaryDatacenter = "dc2"
-
-		c.TLSConfig.GRPC.CAFile = "../../test/hostname/CertAuth.crt"
-		c.TLSConfig.GRPC.CertFile = "../../test/hostname/Betty.crt"
-		c.TLSConfig.GRPC.KeyFile = "../../test/hostname/Betty.key"
 	})
 	testrpc.WaitForLeader(t, s2.RPC, "dc2")
 
@@ -583,11 +578,11 @@ func TestLeader_Peering_DeferredDeletion(t *testing.T) {
 		t.Skip("too slow for testing.Short")
 	}
 
-	// TODO(peering): Configure with TLS
 	_, s1 := testServerWithConfig(t, func(c *Config) {
 		c.NodeName = "s1.dc1"
 		c.Datacenter = "dc1"
 		c.TLSConfig.Domain = "consul"
+		c.GRPCTLSPort = freeport.GetOne(t)
 	})
 	testrpc.WaitForLeader(t, s1.RPC, "dc1")
 
@@ -662,15 +657,21 @@ func TestLeader_Peering_DialerReestablishesConnectionOnError(t *testing.T) {
 	}
 
 	// Reserve a gRPC port so we can restart the accepting server with the same port.
-	ports := freeport.GetN(t, 1)
-	acceptingServerPort := ports[0]
+	acceptingServerPort := freeport.GetOne(t)
 
+	ca := connect.TestCA(t, nil)
 	_, acceptingServer := testServerWithConfig(t, func(c *Config) {
 		c.NodeName = "acceptingServer.dc1"
 		c.Datacenter = "dc1"
-		c.TLSConfig.Domain = "consul"
-		c.GRPCPort = acceptingServerPort
-		c.PeeringEnabled = true
+		c.GRPCTLSPort = acceptingServerPort
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
+		}
 	})
 	testrpc.WaitForLeader(t, acceptingServer.RPC, "dc1")
 
@@ -773,9 +774,17 @@ func TestLeader_Peering_DialerReestablishesConnectionOnError(t *testing.T) {
 		c.NodeName = "acceptingServer.dc1"
 		c.Datacenter = "dc1"
 		c.TLSConfig.Domain = "consul"
-		c.GRPCPort = acceptingServerPort
 		c.DataDir = acceptingServer.config.DataDir
 		c.NodeID = acceptingServer.config.NodeID
+		c.GRPCTLSPort = acceptingServerPort
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
+		}
 	})
 
 	testrpc.WaitForLeader(t, acceptingServerRestart.RPC, "dc1")
@@ -870,11 +879,19 @@ func TestLeader_Peering_ImportedExportedServicesCount(t *testing.T) {
 		t.Skip("too slow for testing.Short")
 	}
 
+	ca := connect.TestCA(t, nil)
 	_, s1 := testServerWithConfig(t, func(c *Config) {
 		c.NodeName = "s1.dc1"
 		c.Datacenter = "dc1"
-		c.TLSConfig.Domain = "consul"
-		c.PeeringEnabled = true
+		c.GRPCTLSPort = freeport.GetOne(t)
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
+		}
 	})
 	testrpc.WaitForLeader(t, s1.RPC, "dc1")
 
@@ -1172,11 +1189,19 @@ func TestLeader_PeeringMetrics_emitPeeringMetrics(t *testing.T) {
 		lastIdx            = uint64(0)
 	)
 
-	// TODO(peering): Configure with TLS
+	ca := connect.TestCA(t, nil)
 	_, s1 := testServerWithConfig(t, func(c *Config) {
 		c.NodeName = "s1.dc1"
 		c.Datacenter = "dc1"
-		c.TLSConfig.Domain = "consul"
+		c.GRPCTLSPort = freeport.GetOne(t)
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
+		}
 	})
 	testrpc.WaitForLeader(t, s1.RPC, "dc1")
 
@@ -1583,10 +1608,20 @@ func Test_Leader_PeeringSync_ServerAddressUpdates(t *testing.T) {
 	maxRetryBackoff = 1
 	t.Cleanup(func() { maxRetryBackoff = orig })
 
+	ca := connect.TestCA(t, nil)
 	_, acceptor := testServerWithConfig(t, func(c *Config) {
 		c.NodeName = "acceptor"
 		c.Datacenter = "dc1"
 		c.TLSConfig.Domain = "consul"
+		c.GRPCTLSPort = freeport.GetOne(t)
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
+		}
 	})
 	testrpc.WaitForLeader(t, acceptor.RPC, "dc1")
 
diff --git a/agent/consul/peering_backend.go b/agent/consul/peering_backend.go
index 8ed8a6079f..26c2f19436 100644
--- a/agent/consul/peering_backend.go
+++ b/agent/consul/peering_backend.go
@@ -9,12 +9,14 @@ import (
 
 	"github.com/hashicorp/consul/acl"
 	"github.com/hashicorp/consul/acl/resolver"
+	"github.com/hashicorp/consul/agent/connect"
 	"github.com/hashicorp/consul/agent/consul/state"
 	"github.com/hashicorp/consul/agent/consul/stream"
 	"github.com/hashicorp/consul/agent/grpc-external/services/peerstream"
 	"github.com/hashicorp/consul/agent/rpc/peering"
 	"github.com/hashicorp/consul/agent/structs"
 	"github.com/hashicorp/consul/ipaddr"
+	"github.com/hashicorp/consul/lib"
 	"github.com/hashicorp/consul/proto/pbpeering"
 )
 
@@ -53,10 +55,34 @@ func (b *PeeringBackend) GetLeaderAddress() string {
 	return b.leaderAddr
 }
 
-// GetAgentCACertificates gets the server's raw CA data from its TLS Configurator.
-func (b *PeeringBackend) GetAgentCACertificates() ([]string, error) {
-	// TODO(peering): handle empty CA pems
-	return b.srv.tlsConfigurator.GRPCManualCAPems(), nil
+// GetTLSMaterials returns the TLS materials for the dialer to dial the acceptor using TLS.
+// It returns the server name to validate, and the CA certificate to validate with.
+func (b *PeeringBackend) GetTLSMaterials(generatingToken bool) (string, []string, error) {
+	if generatingToken {
+		if !b.srv.config.ConnectEnabled {
+			return "", nil, fmt.Errorf("connect.enabled must be set to true in the server's configuration when generating peering tokens")
+		}
+		if b.srv.config.GRPCTLSPort <= 0 && !b.srv.tlsConfigurator.GRPCServerUseTLS() {
+			return "", nil, fmt.Errorf("TLS for gRPC must be enabled when generating peering tokens")
+		}
+	}
+
+	roots, err := b.srv.getCARoots(nil, b.srv.fsm.State())
+	if err != nil {
+		return "", nil, fmt.Errorf("failed to fetch roots: %w", err)
+	}
+	if len(roots.Roots) == 0 || roots.TrustDomain == "" {
+		return "", nil, fmt.Errorf("CA has not finished initializing")
+	}
+
+	serverName := connect.PeeringServerSAN(b.srv.config.Datacenter, roots.TrustDomain)
+
+	var caPems []string
+	for _, r := range roots.Roots {
+		caPems = append(caPems, lib.EnsureTrailingNewline(r.RootCert))
+	}
+
+	return serverName, caPems, nil
 }
 
 // GetServerAddresses looks up server or mesh gateway addresses from the state store.
@@ -117,12 +143,6 @@ func serverAddresses(state *state.Store) ([]string, error) {
 	return addrs, nil
 }
 
-// GetServerName returns the SNI to be returned in the peering token data which
-// will be used by peers when establishing peering connections over TLS.
-func (b *PeeringBackend) GetServerName() string {
-	return b.srv.tlsConfigurator.ServerSNI(b.srv.config.Datacenter, "")
-}
-
 // EncodeToken encodes a peering token as a bas64-encoded representation of JSON (for now).
 func (b *PeeringBackend) EncodeToken(tok *structs.PeeringToken) ([]byte, error) {
 	jsonToken, err := json.Marshal(tok)
diff --git a/agent/consul/peering_backend_oss_test.go b/agent/consul/peering_backend_oss_test.go
index 3c120d26f7..11466581b3 100644
--- a/agent/consul/peering_backend_oss_test.go
+++ b/agent/consul/peering_backend_oss_test.go
@@ -11,7 +11,10 @@ import (
 	"github.com/stretchr/testify/require"
 	gogrpc "google.golang.org/grpc"
 
+	"github.com/hashicorp/consul/agent/connect"
+	"github.com/hashicorp/consul/agent/structs"
 	"github.com/hashicorp/consul/proto/pbpeering"
+	"github.com/hashicorp/consul/sdk/freeport"
 	"github.com/hashicorp/consul/testrpc"
 )
 
@@ -21,9 +24,18 @@ func TestPeeringBackend_RejectsPartition(t *testing.T) {
 	}
 
 	t.Parallel()
+
+	ca := connect.TestCA(t, nil)
 	_, s1 := testServerWithConfig(t, func(c *Config) {
-		c.Datacenter = "dc1"
-		c.Bootstrap = true
+		c.GRPCTLSPort = freeport.GetOne(t)
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
+		}
 	})
 
 	testrpc.WaitForLeader(t, s1.RPC, "dc1")
@@ -55,9 +67,17 @@ func TestPeeringBackend_IgnoresDefaultPartition(t *testing.T) {
 	}
 
 	t.Parallel()
+	ca := connect.TestCA(t, nil)
 	_, s1 := testServerWithConfig(t, func(c *Config) {
-		c.Datacenter = "dc1"
-		c.Bootstrap = true
+		c.GRPCTLSPort = freeport.GetOne(t)
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
+		}
 	})
 
 	testrpc.WaitForLeader(t, s1.RPC, "dc1")
diff --git a/agent/consul/peering_backend_test.go b/agent/consul/peering_backend_test.go
index 2d9b9f029d..0d834c09a9 100644
--- a/agent/consul/peering_backend_test.go
+++ b/agent/consul/peering_backend_test.go
@@ -7,17 +7,18 @@ import (
 	"testing"
 	"time"
 
-	"github.com/hashicorp/consul/agent/structs"
-	"github.com/hashicorp/consul/sdk/freeport"
-	"github.com/hashicorp/consul/types"
-	"github.com/stretchr/testify/require"
 	gogrpc "google.golang.org/grpc"
 
+	"github.com/hashicorp/consul/agent/connect"
 	"github.com/hashicorp/consul/agent/pool"
+	"github.com/hashicorp/consul/agent/structs"
 	"github.com/hashicorp/consul/proto/pbpeering"
 	"github.com/hashicorp/consul/proto/pbpeerstream"
+	"github.com/hashicorp/consul/sdk/freeport"
 	"github.com/hashicorp/consul/sdk/testutil"
 	"github.com/hashicorp/consul/testrpc"
+	"github.com/hashicorp/consul/types"
+	"github.com/stretchr/testify/require"
 )
 
 func TestPeeringBackend_ForwardToLeader(t *testing.T) {
@@ -25,17 +26,26 @@ func TestPeeringBackend_ForwardToLeader(t *testing.T) {
 		t.Skip("too slow for testing.Short")
 	}
 
-	_, conf1 := testServerConfig(t)
-	server1, err := newServer(t, conf1)
-	require.NoError(t, err)
-
-	_, conf2 := testServerConfig(t)
-	conf2.Bootstrap = false
-	server2, err := newServer(t, conf2)
-	require.NoError(t, err)
+	ca := connect.TestCA(t, nil)
+	_, server1 := testServerWithConfig(t, func(c *Config) {
+		c.GRPCTLSPort = freeport.GetOne(t)
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
+		}
+	})
+	_, server2 := testServerWithConfig(t, func(c *Config) {
+		c.Bootstrap = false
+	})
 
 	// Join a 2nd server (not the leader)
 	testrpc.WaitForLeader(t, server1.RPC, "dc1")
+	testrpc.WaitForActiveCARoot(t, server1.RPC, "dc1", nil)
+
 	joinLAN(t, server2, server1)
 	testrpc.WaitForLeader(t, server2.RPC, "dc1")
 
@@ -166,17 +176,26 @@ func TestPeerStreamService_ForwardToLeader(t *testing.T) {
 		t.Skip("too slow for testing.Short")
 	}
 
-	_, conf1 := testServerConfig(t)
-	server1, err := newServer(t, conf1)
-	require.NoError(t, err)
-
-	_, conf2 := testServerConfig(t)
-	conf2.Bootstrap = false
-	server2, err := newServer(t, conf2)
-	require.NoError(t, err)
+	ca := connect.TestCA(t, nil)
+	_, server1 := testServerWithConfig(t, func(c *Config) {
+		c.GRPCTLSPort = freeport.GetOne(t)
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
+		}
+	})
+	_, server2 := testServerWithConfig(t, func(c *Config) {
+		c.Bootstrap = false
+	})
 
 	// server1 is leader, server2 follower
 	testrpc.WaitForLeader(t, server1.RPC, "dc1")
+	testrpc.WaitForActiveCARoot(t, server1.RPC, "dc1", nil)
+
 	joinLAN(t, server2, server1)
 	testrpc.WaitForLeader(t, server2.RPC, "dc1")
 
diff --git a/agent/consul/prepared_query_endpoint_test.go b/agent/consul/prepared_query_endpoint_test.go
index 07e9801a68..108a568498 100644
--- a/agent/consul/prepared_query_endpoint_test.go
+++ b/agent/consul/prepared_query_endpoint_test.go
@@ -21,12 +21,14 @@ import (
 	"github.com/hashicorp/consul-net-rpc/net/rpc"
 
 	"github.com/hashicorp/consul/acl"
+	"github.com/hashicorp/consul/agent/connect"
 	grpcexternal "github.com/hashicorp/consul/agent/grpc-external"
 	"github.com/hashicorp/consul/agent/structs"
 	"github.com/hashicorp/consul/agent/structs/aclfilter"
 	tokenStore "github.com/hashicorp/consul/agent/token"
 	"github.com/hashicorp/consul/api"
 	"github.com/hashicorp/consul/proto/pbpeering"
+	"github.com/hashicorp/consul/sdk/freeport"
 	"github.com/hashicorp/consul/sdk/testutil/retry"
 	"github.com/hashicorp/consul/testrpc"
 	"github.com/hashicorp/consul/types"
@@ -1463,10 +1465,20 @@ func TestPreparedQuery_Execute(t *testing.T) {
 
 	s2.tokens.UpdateReplicationToken("root", tokenStore.TokenSourceConfig)
 
+	ca := connect.TestCA(t, nil)
 	dir3, s3 := testServerWithConfig(t, func(c *Config) {
 		c.Datacenter = "dc3"
 		c.PrimaryDatacenter = "dc3"
 		c.NodeName = "acceptingServer.dc3"
+		c.GRPCTLSPort = freeport.GetOne(t)
+		c.CAConfig = &structs.CAConfiguration{
+			ClusterID: connect.TestClusterID,
+			Provider:  structs.ConsulCAProvider,
+			Config: map[string]interface{}{
+				"PrivateKey": ca.SigningKey,
+				"RootCert":   ca.RootCert,
+			},
+		}
 	})
 	defer os.RemoveAll(dir3)
 	defer s3.Shutdown()
diff --git a/agent/consul/server_test.go b/agent/consul/server_test.go
index 287dca871b..b9f8e7db90 100644
--- a/agent/consul/server_test.go
+++ b/agent/consul/server_test.go
@@ -232,7 +232,7 @@ func testServerWithConfig(t *testing.T, configOpts ...func(*Config)) (string, *S
 		}
 
 		// Apply config to copied fields because many tests only set the old
-		//values.
+		// values.
 		config.ACLResolverSettings.ACLsEnabled = config.ACLsEnabled
 		config.ACLResolverSettings.NodeName = config.NodeName
 		config.ACLResolverSettings.Datacenter = config.Datacenter
@@ -247,15 +247,32 @@ func testServerWithConfig(t *testing.T, configOpts ...func(*Config)) (string, *S
 	})
 	t.Cleanup(func() { srv.Shutdown() })
 
-	if srv.config.GRPCPort > 0 {
+	for _, grpcPort := range []int{srv.config.GRPCPort, srv.config.GRPCTLSPort} {
+		if grpcPort == 0 {
+			continue
+		}
+
 		// Normally the gRPC server listener is created at the agent level and
 		// passed down into the Server creation.
-		externalGRPCAddr := fmt.Sprintf("127.0.0.1:%d", srv.config.GRPCPort)
-		ln, err := net.Listen("tcp", externalGRPCAddr)
+		ln, err := net.Listen("tcp", fmt.Sprintf("127.0.0.1:%d", grpcPort))
 		require.NoError(t, err)
 
-		// Wrap the listener with TLS
-		if deps.TLSConfigurator.GRPCServerUseTLS() {
+		if grpcPort == srv.config.GRPCTLSPort || deps.TLSConfigurator.GRPCServerUseTLS() {
+			// Set the internally managed server certificate. The cert manager is hooked to the Agent, so we need to bypass that here.
+			if srv.config.PeeringEnabled && srv.config.ConnectEnabled {
+				key, _ := srv.config.CAConfig.Config["PrivateKey"].(string)
+				cert, _ := srv.config.CAConfig.Config["RootCert"].(string)
+				if key != "" && cert != "" {
+					ca := &structs.CARoot{
+						SigningKey: key,
+						RootCert:   cert,
+					}
+					require.NoError(t, deps.TLSConfigurator.UpdateAutoTLSCert(connect.TestServerLeaf(t, srv.config.Datacenter, ca)))
+					deps.TLSConfigurator.UpdateAutoTLSPeeringServerName(connect.PeeringServerSAN("dc1", connect.TestTrustDomain))
+				}
+			}
+
+			// Wrap the listener with TLS.
 			ln = tls.NewListener(ln, deps.TLSConfigurator.IncomingGRPCConfig())
 		}
 
diff --git a/agent/grpc-external/services/peerstream/stream_test.go b/agent/grpc-external/services/peerstream/stream_test.go
index 156efa4759..da167bd2a6 100644
--- a/agent/grpc-external/services/peerstream/stream_test.go
+++ b/agent/grpc-external/services/peerstream/stream_test.go
@@ -43,7 +43,6 @@ import (
 
 const (
 	testPeerID                = "caf067a6-f112-4907-9101-d45857d2b149"
-	testActiveStreamSecretID  = "e778c518-f0db-473a-9224-24b357da971d"
 	testPendingStreamSecretID = "522c0daf-2ef2-4dab-bc78-5e04e3daf552"
 	testEstablishmentSecretID = "f6569d37-1c5b-4415-aae5-26f4594f7f60"
 )
diff --git a/agent/peering_endpoint_test.go b/agent/peering_endpoint_test.go
index 0f5692bad1..c7006a9259 100644
--- a/agent/peering_endpoint_test.go
+++ b/agent/peering_endpoint_test.go
@@ -22,25 +22,6 @@ import (
 	"github.com/hashicorp/consul/testrpc"
 )
 
-var validCA = `
------BEGIN CERTIFICATE-----
-MIICmDCCAj6gAwIBAgIBBzAKBggqhkjOPQQDAjAWMRQwEgYDVQQDEwtDb25zdWwg
-Q0EgNzAeFw0xODA1MjExNjMzMjhaFw0yODA1MTgxNjMzMjhaMBYxFDASBgNVBAMT
-C0NvbnN1bCBDQSA3MFkwEwYHKoZIzj0CAQYIKoZIzj0DAQcDQgAER0qlxjnRcMEr
-iSGlH7G7dYU7lzBEmLUSMZkyBbClmyV8+e8WANemjn+PLnCr40If9cmpr7RnC9Qk
-GTaLnLiF16OCAXswggF3MA4GA1UdDwEB/wQEAwIBhjAPBgNVHRMBAf8EBTADAQH/
-MGgGA1UdDgRhBF8xZjo5MTpjYTo0MTo4ZjphYzo2NzpiZjo1OTpjMjpmYTo0ZTo3
-NTo1YzpkODpmMDo1NTpkZTpiZTo3NTpiODozMzozMTpkNToyNDpiMDowNDpiMzpl
-ODo5Nzo1Yjo3ZTBqBgNVHSMEYzBhgF8xZjo5MTpjYTo0MTo4ZjphYzo2NzpiZjo1
-OTpjMjpmYTo0ZTo3NTo1YzpkODpmMDo1NTpkZTpiZTo3NTpiODozMzozMTpkNToy
-NDpiMDowNDpiMzplODo5Nzo1Yjo3ZTA/BgNVHREEODA2hjRzcGlmZmU6Ly8xMjRk
-ZjVhMC05ODIwLTc2YzMtOWFhOS02ZjYyMTY0YmExYzIuY29uc3VsMD0GA1UdHgEB
-/wQzMDGgLzAtgisxMjRkZjVhMC05ODIwLTc2YzMtOWFhOS02ZjYyMTY0YmExYzIu
-Y29uc3VsMAoGCCqGSM49BAMCA0gAMEUCIQDzkkI7R+0U12a+zq2EQhP/n2mHmta+
-fs2hBxWIELGwTAIgLdO7RRw+z9nnxCIA6kNl//mIQb+PGItespiHZKAz74Q=
------END CERTIFICATE-----
-`
-
 func TestHTTP_Peering_GenerateToken(t *testing.T) {
 	if testing.Short() {
 		t.Skip("too slow for testing.Short")
@@ -50,6 +31,7 @@ func TestHTTP_Peering_GenerateToken(t *testing.T) {
 	a := NewTestAgent(t, "")
 
 	testrpc.WaitForTestAgent(t, a.RPC, "dc1")
+	testrpc.WaitForActiveCARoot(t, a.RPC, "dc1", nil)
 
 	t.Run("No Body", func(t *testing.T) {
 		req, err := http.NewRequest("POST", "/v1/peering/token", nil)
@@ -107,9 +89,9 @@ func TestHTTP_Peering_GenerateToken(t *testing.T) {
 		var token structs.PeeringToken
 		require.NoError(t, json.Unmarshal(tokenJSON, &token))
 
-		require.Nil(t, token.CA)
-		require.Equal(t, []string{fmt.Sprintf("127.0.0.1:%d", a.config.GRPCPort)}, token.ServerAddresses)
-		require.Equal(t, "server.dc1.consul", token.ServerName)
+		require.NotNil(t, token.CA)
+		require.Equal(t, []string{fmt.Sprintf("127.0.0.1:%d", a.config.GRPCTLSPort)}, token.ServerAddresses)
+		require.Equal(t, "server.dc1.peering.11111111-2222-3333-4444-555555555555.consul", token.ServerName)
 
 		// The PeerID in the token is randomly generated so we don't assert on its value.
 		require.NotEmpty(t, token.PeerID)
@@ -140,9 +122,9 @@ func TestHTTP_Peering_GenerateToken(t *testing.T) {
 		var token structs.PeeringToken
 		require.NoError(t, json.Unmarshal(tokenJSON, &token))
 
-		require.Nil(t, token.CA)
+		require.NotNil(t, token.CA)
 		require.Equal(t, []string{externalAddress}, token.ServerAddresses)
-		require.Equal(t, "server.dc1.consul", token.ServerName)
+		require.Equal(t, "server.dc1.peering.11111111-2222-3333-4444-555555555555.consul", token.ServerName)
 
 		// The PeerID in the token is randomly generated so we don't assert on its value.
 		require.NotEmpty(t, token.PeerID)
@@ -159,6 +141,7 @@ func TestHTTP_Peering_GenerateToken_EdgeCases(t *testing.T) {
 
 	a := NewTestAgent(t, "")
 	testrpc.WaitForTestAgent(t, a.RPC, "dc1")
+	testrpc.WaitForActiveCARoot(t, a.RPC, "dc1", nil)
 
 	body := &pbpeering.GenerateTokenRequest{
 		PeerName: "peering-a",
@@ -219,10 +202,9 @@ func TestHTTP_Peering_Establish(t *testing.T) {
 		t.Skip("too slow for testing.Short")
 	}
 
-	t.Parallel()
 	a := NewTestAgent(t, "")
-
 	testrpc.WaitForTestAgent(t, a.RPC, "dc1")
+	testrpc.WaitForActiveCARoot(t, a.RPC, "dc1", nil)
 
 	t.Run("No Body", func(t *testing.T) {
 		req, err := http.NewRequest("POST", "/v1/peering/establish", nil)
@@ -291,14 +273,17 @@ func TestHTTP_Peering_Establish(t *testing.T) {
 		})
 		require.NoError(t, err)
 
-		req, err = http.NewRequest("POST", "/v1/peering/establish", bytes.NewReader(b))
-		require.NoError(t, err)
-		resp = httptest.NewRecorder()
-		a2.srv.h.ServeHTTP(resp, req)
-		require.Equal(t, http.StatusOK, resp.Code, "expected 200, got %d: %v", resp.Code, resp.Body.String())
+		retry.Run(t, func(r *retry.R) {
+			req, err = http.NewRequest("POST", "/v1/peering/establish", bytes.NewReader(b))
+			require.NoError(r, err)
 
-		// success response does not currently return a value so {} is correct
-		require.Equal(t, "{}", resp.Body.String())
+			resp = httptest.NewRecorder()
+			a2.srv.h.ServeHTTP(resp, req)
+			require.Equal(r, http.StatusOK, resp.Code, "expected 200, got %d: %v", resp.Code, resp.Body.String())
+
+			// success response does not currently return a value so {} is correct
+			require.Equal(r, "{}", resp.Body.String())
+		})
 	})
 }
 
@@ -416,6 +401,7 @@ func TestHTTP_Peering_Delete(t *testing.T) {
 	a := NewTestAgent(t, "")
 
 	testrpc.WaitForTestAgent(t, a.RPC, "dc1")
+	testrpc.WaitForActiveCARoot(t, a.RPC, "dc1", nil)
 
 	bodyBytes, err := json.Marshal(&pbpeering.GenerateTokenRequest{
 		PeerName: "foo",
diff --git a/agent/rpc/peering/service.go b/agent/rpc/peering/service.go
index daef4ef3a0..aa3e4412ca 100644
--- a/agent/rpc/peering/service.go
+++ b/agent/rpc/peering/service.go
@@ -114,17 +114,14 @@ type Backend interface {
 	// partition and namespace from the token.
 	ResolveTokenAndDefaultMeta(token string, entMeta *acl.EnterpriseMeta, authzCtx *acl.AuthorizerContext) (resolver.Result, error)
 
-	// GetAgentCACertificates returns the CA certificate to be returned in the peering token data
-	GetAgentCACertificates() ([]string, error)
+	// GetTLSMaterials returns the TLS materials for the dialer to dial the acceptor using TLS.
+	// It returns the server name to validate, and the CA certificate to validate with.
+	GetTLSMaterials(generatingToken bool) (string, []string, error)
 
 	// GetServerAddresses returns the addresses used for establishing a peering connection.
 	// These may be server addresses or mesh gateway addresses if peering through mesh gateways.
 	GetServerAddresses() ([]string, error)
 
-	// GetServerName returns the SNI to be returned in the peering token data which
-	// will be used by peers when establishing peering connections over TLS.
-	GetServerName() string
-
 	// EncodeToken packages a peering token into a slice of bytes.
 	EncodeToken(tok *structs.PeeringToken) ([]byte, error)
 
@@ -224,6 +221,11 @@ func (s *Server) GenerateToken(
 		return nil, err
 	}
 
+	serverName, caPEMs, err := s.Backend.GetTLSMaterials(true)
+	if err != nil {
+		return nil, err
+	}
+
 	var (
 		peering  *pbpeering.Peering
 		secretID string
@@ -291,11 +293,6 @@ func (s *Server) GenerateToken(
 		break
 	}
 
-	ca, err := s.Backend.GetAgentCACertificates()
-	if err != nil {
-		return nil, err
-	}
-
 	// ServerExternalAddresses must be formatted as addr:port.
 	var serverAddrs []string
 	if len(req.ServerExternalAddresses) > 0 {
@@ -310,9 +307,9 @@ func (s *Server) GenerateToken(
 	tok := structs.PeeringToken{
 		// Store the UUID so that we can do a global search when handling inbound streams.
 		PeerID:              peering.ID,
-		CA:                  ca,
+		CA:                  caPEMs,
 		ServerAddresses:     serverAddrs,
-		ServerName:          s.Backend.GetServerName(),
+		ServerName:          serverName,
 		EstablishmentSecret: secretID,
 	}
 
@@ -487,8 +484,13 @@ func (s *Server) validatePeeringLocality(token *structs.PeeringToken, partition
 
 	// If the token has the same server name as this cluster, but we can't find the peering
 	// in our store, it indicates a naming conflict.
-	if s.Backend.GetServerName() == token.ServerName && peering == nil {
-		return fmt.Errorf("conflict - peering token's server name matches the current cluster's server name, %q, but there is no record in the database", s.Backend.GetServerName())
+	serverName, _, err := s.Backend.GetTLSMaterials(false)
+	if err != nil {
+		return fmt.Errorf("failed to fetch TLS materials: %w", err)
+	}
+
+	if serverName == token.ServerName && peering == nil {
+		return fmt.Errorf("conflict - peering token's server name matches the current cluster's server name, %q, but there is no record in the database", serverName)
 	}
 
 	if peering != nil && acl.EqualPartitions(peering.GetPartition(), partition) {
diff --git a/agent/rpc/peering/service_test.go b/agent/rpc/peering/service_test.go
index e0d29b2725..ae822c24aa 100644
--- a/agent/rpc/peering/service_test.go
+++ b/agent/rpc/peering/service_test.go
@@ -2,6 +2,7 @@ package peering_test
 
 import (
 	"context"
+	"crypto/tls"
 	"encoding/base64"
 	"encoding/json"
 	"fmt"
@@ -19,6 +20,7 @@ import (
 	grpcstatus "google.golang.org/grpc/status"
 
 	"github.com/hashicorp/consul/acl"
+	"github.com/hashicorp/consul/agent/connect"
 	"github.com/hashicorp/consul/agent/consul"
 	"github.com/hashicorp/consul/agent/consul/state"
 	"github.com/hashicorp/consul/agent/consul/stream"
@@ -62,6 +64,7 @@ func generateTooManyMetaKeys() map[string]string {
 
 func TestPeeringService_GenerateToken(t *testing.T) {
 	dir := testutil.TempDir(t, "consul")
+
 	signer, _, _ := tlsutil.GeneratePrivateKey()
 	ca, _, _ := tlsutil.GenerateCA(tlsutil.CAOpts{Signer: signer})
 	cafile := path.Join(dir, "cacert.pem")
@@ -97,10 +100,14 @@ func TestPeeringService_GenerateToken(t *testing.T) {
 
 		token := &structs.PeeringToken{}
 		require.NoError(t, json.Unmarshal(tokenJSON, token))
-		require.Equal(t, "server.dc1.consul", token.ServerName)
+		require.Equal(t, "server.dc1.peering.11111111-2222-3333-4444-555555555555.consul", token.ServerName)
 		require.Len(t, token.ServerAddresses, 1)
 		require.Equal(t, s.PublicGRPCAddr, token.ServerAddresses[0])
-		require.Equal(t, []string{ca}, token.CA)
+
+		// The roots utilized should be the ConnectCA roots and not the ones manually configured.
+		_, roots, err := s.Server.FSM().State().CARoots(nil)
+		require.NoError(t, err)
+		require.Equal(t, []string{roots.Active().RootCert}, token.CA)
 
 		require.NotEmpty(t, token.EstablishmentSecret)
 		secret = token.EstablishmentSecret
@@ -165,6 +172,7 @@ func TestPeeringService_GenerateToken(t *testing.T) {
 
 func TestPeeringService_GenerateTokenExternalAddress(t *testing.T) {
 	dir := testutil.TempDir(t, "consul")
+
 	signer, _, _ := tlsutil.GeneratePrivateKey()
 	ca, _, _ := tlsutil.GenerateCA(tlsutil.CAOpts{Signer: signer})
 	cafile := path.Join(dir, "cacert.pem")
@@ -191,10 +199,14 @@ func TestPeeringService_GenerateTokenExternalAddress(t *testing.T) {
 
 	token := &structs.PeeringToken{}
 	require.NoError(t, json.Unmarshal(tokenJSON, token))
-	require.Equal(t, "server.dc1.consul", token.ServerName)
+	require.Equal(t, "server.dc1.peering.11111111-2222-3333-4444-555555555555.consul", token.ServerName)
 	require.Len(t, token.ServerAddresses, 1)
 	require.Equal(t, externalAddress, token.ServerAddresses[0])
-	require.Equal(t, []string{ca}, token.CA)
+
+	// The roots utilized should be the ConnectCA roots and not the ones manually configured.
+	_, roots, err := s.Server.FSM().State().CARoots(nil)
+	require.NoError(t, err)
+	require.Equal(t, []string{roots.Active().RootCert}, token.CA)
 }
 
 func TestPeeringService_GenerateToken_ACLEnforcement(t *testing.T) {
@@ -385,9 +397,13 @@ func TestPeeringService_Establish_serverNameConflict(t *testing.T) {
 	// Manufacture token to have the same server name but a PeerID not in the store.
 	id, err := uuid.GenerateUUID()
 	require.NoError(t, err, "could not generate uuid")
+
+	serverName, _, err := s.Server.GetPeeringBackend().GetTLSMaterials(true)
+	require.NoError(t, err)
+
 	peeringToken := structs.PeeringToken{
 		ServerAddresses:     []string{"1.2.3.4:8502"},
-		ServerName:          s.Server.GetPeeringBackend().GetServerName(),
+		ServerName:          serverName,
 		EstablishmentSecret: "foo",
 		PeerID:              id,
 	}
@@ -409,12 +425,15 @@ func TestPeeringService_Establish_serverNameConflict(t *testing.T) {
 
 func TestPeeringService_Establish(t *testing.T) {
 	// TODO(peering): see note on newTestServer, refactor to not use this
-	s1 := newTestServer(t, nil)
+	s1 := newTestServer(t, func(conf *consul.Config) {
+		conf.NodeName = "s1"
+	})
 	client1 := pbpeering.NewPeeringServiceClient(s1.ClientConn(t))
 
 	s2 := newTestServer(t, func(conf *consul.Config) {
+		conf.NodeName = "s2"
 		conf.Datacenter = "dc2"
-		conf.GRPCPort = 5301
+		conf.PrimaryDatacenter = "dc2"
 	})
 	client2 := pbpeering.NewPeeringServiceClient(s2.ClientConn(t))
 
@@ -430,8 +449,10 @@ func TestPeeringService_Establish(t *testing.T) {
 
 	var peerID string
 	testutil.RunStep(t, "peering can be established from token", func(t *testing.T) {
-		_, err = client2.Establish(ctx, &pbpeering.EstablishRequest{PeerName: "my-peer-s1", PeeringToken: tokenResp.PeeringToken})
-		require.NoError(t, err)
+		retry.Run(t, func(r *retry.R) {
+			_, err = client2.Establish(ctx, &pbpeering.EstablishRequest{PeerName: "my-peer-s1", PeeringToken: tokenResp.PeeringToken})
+			require.NoError(r, err)
+		})
 
 		ctx, cancel = context.WithTimeout(context.Background(), 10*time.Second)
 		t.Cleanup(cancel)
@@ -1097,9 +1118,7 @@ func TestPeeringService_TrustBundleListByService(t *testing.T) {
 }
 
 func TestPeeringService_validatePeer(t *testing.T) {
-	s1 := newTestServer(t, func(c *consul.Config) {
-		c.SerfLANConfig.MemberlistConfig.AdvertiseAddr = "127.0.0.1"
-	})
+	s1 := newTestServer(t, nil)
 	client1 := pbpeering.NewPeeringServiceClient(s1.ClientConn(t))
 
 	ctx, cancel := context.WithTimeout(context.Background(), 10*time.Second)
@@ -1113,8 +1132,8 @@ func TestPeeringService_validatePeer(t *testing.T) {
 	})
 
 	s2 := newTestServer(t, func(conf *consul.Config) {
-		conf.GRPCPort = 5301
 		conf.Datacenter = "dc2"
+		conf.PrimaryDatacenter = "dc2"
 	})
 	client2 := pbpeering.NewPeeringServiceClient(s2.ClientConn(t))
 
@@ -1364,7 +1383,18 @@ func newTestServer(t *testing.T, cb func(conf *consul.Config)) testingServer {
 	conf.PrimaryDatacenter = "dc1"
 	conf.ConnectEnabled = true
 
-	conf.GRPCPort = ports[3]
+	ca := connect.TestCA(t, nil)
+	conf.CAConfig = &structs.CAConfiguration{
+		ClusterID: connect.TestClusterID,
+		Provider:  structs.ConsulCAProvider,
+		Config: map[string]interface{}{
+			"PrivateKey":          ca.SigningKey,
+			"RootCert":            ca.RootCert,
+			"LeafCertTTL":         "72h",
+			"IntermediateCertTTL": "288h",
+		},
+	}
+	conf.GRPCTLSPort = ports[3]
 
 	nodeID, err := uuid.GenerateUUID()
 	if err != nil {
@@ -1383,27 +1413,34 @@ func newTestServer(t *testing.T, cb func(conf *consul.Config)) testingServer {
 	conf.ACLResolverSettings.Datacenter = conf.Datacenter
 	conf.ACLResolverSettings.EnterpriseMeta = *conf.AgentEnterpriseMeta()
 
-	externalGRPCServer := gogrpc.NewServer()
-
 	deps := newDefaultDeps(t, conf)
+	externalGRPCServer := external.NewServer(deps.Logger)
+
 	server, err := consul.NewServer(conf, deps, externalGRPCServer)
 	require.NoError(t, err)
 	t.Cleanup(func() {
 		require.NoError(t, server.Shutdown())
 	})
 
+	require.NoError(t, deps.TLSConfigurator.UpdateAutoTLSCert(connect.TestServerLeaf(t, conf.Datacenter, ca)))
+	deps.TLSConfigurator.UpdateAutoTLSPeeringServerName(connect.PeeringServerSAN(conf.Datacenter, connect.TestTrustDomain))
+
 	// Normally the gRPC server listener is created at the agent level and
 	// passed down into the Server creation.
-	grpcAddr := fmt.Sprintf("127.0.0.1:%d", conf.GRPCPort)
+	grpcAddr := fmt.Sprintf("127.0.0.1:%d", conf.GRPCTLSPort)
 
 	ln, err := net.Listen("tcp", grpcAddr)
 	require.NoError(t, err)
+
+	ln = tls.NewListener(ln, deps.TLSConfigurator.IncomingGRPCConfig())
+
 	go func() {
 		_ = externalGRPCServer.Serve(ln)
 	}()
 	t.Cleanup(externalGRPCServer.Stop)
 
 	testrpc.WaitForLeader(t, server.RPC, conf.Datacenter)
+	testrpc.WaitForActiveCARoot(t, server.RPC, conf.Datacenter, nil)
 
 	return testingServer{
 		Server:         server,
diff --git a/agent/rpc/peering/validate.go b/agent/rpc/peering/validate.go
index 340e4c5ad7..af415102b1 100644
--- a/agent/rpc/peering/validate.go
+++ b/agent/rpc/peering/validate.go
@@ -38,9 +38,7 @@ func validatePeeringToken(tok *structs.PeeringToken) error {
 		}
 	}
 
-	// TODO(peering): validate name matches SNI?
-	// TODO(peering): validate name well formed?
-	if tok.ServerName == "" {
+	if len(tok.CA) > 0 && tok.ServerName == "" {
 		return errPeeringTokenEmptyServerName
 	}
 
diff --git a/agent/testagent.go b/agent/testagent.go
index 2fb4438ddb..2d34ba198b 100644
--- a/agent/testagent.go
+++ b/agent/testagent.go
@@ -190,7 +190,7 @@ func (a *TestAgent) Start(t *testing.T) error {
 		Name:       name,
 	})
 
-	portsConfig := randomPortsSource(t, a.UseHTTPS, a.UseGRPCTLS)
+	portsConfig := randomPortsSource(t, a.UseHTTPS)
 
 	// Create NodeID outside the closure, so that it does not change
 	testHCLConfig := TestConfigHCL(NodeID())
@@ -412,7 +412,7 @@ func (a *TestAgent) consulConfig() *consul.Config {
 // chance of port conflicts for concurrently executed test binaries.
 // Instead of relying on one set of ports to be sufficient we retry
 // starting the agent with different ports on port conflict.
-func randomPortsSource(t *testing.T, useHTTPS bool, useGRPCTLS bool) string {
+func randomPortsSource(t *testing.T, useHTTPS bool) string {
 	ports := freeport.GetN(t, 8)
 
 	var http, https int
@@ -424,15 +424,6 @@ func randomPortsSource(t *testing.T, useHTTPS bool, useGRPCTLS bool) string {
 		https = -1
 	}
 
-	var grpc, grpcTLS int
-	if useGRPCTLS {
-		grpc = -1
-		grpcTLS = ports[7]
-	} else {
-		grpc = ports[6]
-		grpcTLS = -1
-	}
-
 	return `
 		ports = {
 			dns = ` + strconv.Itoa(ports[0]) + `
@@ -441,8 +432,8 @@ func randomPortsSource(t *testing.T, useHTTPS bool, useGRPCTLS bool) string {
 			serf_lan = ` + strconv.Itoa(ports[3]) + `
 			serf_wan = ` + strconv.Itoa(ports[4]) + `
 			server = ` + strconv.Itoa(ports[5]) + `
-			grpc = ` + strconv.Itoa(grpc) + `
-			grpc_tls = ` + strconv.Itoa(grpcTLS) + `
+			grpc = ` + strconv.Itoa(ports[6]) + `
+			grpc_tls = ` + strconv.Itoa(ports[7]) + `
 		}
 	`
 }
diff --git a/api/api_test.go b/api/api_test.go
index 3574240d1a..e1fabbb135 100644
--- a/api/api_test.go
+++ b/api/api_test.go
@@ -96,6 +96,10 @@ func makeClientWithConfig(
 	if server.Config.Bootstrap {
 		server.WaitForLeader(t)
 	}
+	connectEnabled := server.Config.Connect["enabled"]
+	if enabled, ok := connectEnabled.(bool); ok && server.Config.Server && enabled {
+		server.WaitForActiveCARoot(t)
+	}
 
 	conf.Address = server.HTTPAddr
 
diff --git a/api/peering_test.go b/api/peering_test.go
index 9b7974ea44..eb58f22e40 100644
--- a/api/peering_test.go
+++ b/api/peering_test.go
@@ -44,7 +44,6 @@ func TestAPI_Peering_ACLDeny(t *testing.T) {
 		serverConfig.ACL.Tokens.InitialManagement = "root"
 		serverConfig.ACL.Enabled = true
 		serverConfig.ACL.DefaultPolicy = "deny"
-		serverConfig.Ports.GRPC = 5300
 	})
 	defer s1.Stop()
 
@@ -52,7 +51,6 @@ func TestAPI_Peering_ACLDeny(t *testing.T) {
 		serverConfig.ACL.Tokens.InitialManagement = "root"
 		serverConfig.ACL.Enabled = true
 		serverConfig.ACL.DefaultPolicy = "deny"
-		serverConfig.Ports.GRPC = 5301
 		serverConfig.Datacenter = "dc2"
 	})
 	defer s2.Stop()
@@ -265,7 +263,7 @@ func TestAPI_Peering_GenerateToken_ExternalAddresses(t *testing.T) {
 func TestAPI_Peering_GenerateToken_Read_Establish_Delete(t *testing.T) {
 	t.Parallel()
 
-	c, s := makeClient(t) // this is "dc1"
+	c, s := makeClientWithConfig(t, nil, nil) // this is "dc1"
 	defer s.Stop()
 	s.WaitForSerfCheck(t)
 
diff --git a/command/peering/establish/establish_test.go b/command/peering/establish/establish_test.go
index 4d1d83e364..f24ac2a265 100644
--- a/command/peering/establish/establish_test.go
+++ b/command/peering/establish/establish_test.go
@@ -11,6 +11,7 @@ import (
 
 	"github.com/hashicorp/consul/agent"
 	"github.com/hashicorp/consul/api"
+	"github.com/hashicorp/consul/sdk/testutil/retry"
 	"github.com/hashicorp/consul/testrpc"
 )
 
@@ -84,10 +85,12 @@ func TestEstablishCommand(t *testing.T) {
 			fmt.Sprintf("-peering-token=%s", res.PeeringToken),
 		}
 
-		code := cmd.Run(args)
-		require.Equal(t, 0, code)
-		output := ui.OutputWriter.String()
-		require.Contains(t, output, "Success")
+		retry.Run(t, func(r *retry.R) {
+			code := cmd.Run(args)
+			require.Equal(r, 0, code)
+			output := ui.OutputWriter.String()
+			require.Contains(r, output, "Success")
+		})
 	})
 
 	t.Run("establish connection with options", func(t *testing.T) {
@@ -107,12 +110,14 @@ func TestEstablishCommand(t *testing.T) {
 			"-meta=region=us-west-1",
 		}
 
-		code := cmd.Run(args)
-		require.Equal(t, 0, code)
-		output := ui.OutputWriter.String()
-		require.Contains(t, output, "Success")
+		retry.Run(t, func(r *retry.R) {
+			code := cmd.Run(args)
+			require.Equal(r, 0, code)
+			output := ui.OutputWriter.String()
+			require.Contains(r, output, "Success")
+		})
 
-		//Meta
+		// Meta
 		peering, _, err := dialingClient.Peerings().Read(context.Background(), "bar", &api.QueryOptions{})
 		require.NoError(t, err)
 
diff --git a/command/peering/generate/generate_test.go b/command/peering/generate/generate_test.go
index c745976104..b23d664d84 100644
--- a/command/peering/generate/generate_test.go
+++ b/command/peering/generate/generate_test.go
@@ -78,7 +78,7 @@ func TestGenerateCommand(t *testing.T) {
 		require.Equal(t, 0, code)
 		token, err := base64.StdEncoding.DecodeString(ui.OutputWriter.String())
 		require.NoError(t, err, "error decoding token")
-		require.Contains(t, string(token), "\"ServerName\":\"server.dc1.consul\"")
+		require.Contains(t, string(token), "\"ServerName\":\"server.dc1.peering.11111111-2222-3333-4444-555555555555.consul\"")
 	})
 
 	t.Run("generate token with options", func(t *testing.T) {
@@ -97,13 +97,13 @@ func TestGenerateCommand(t *testing.T) {
 		require.Equal(t, 0, code)
 		token, err := base64.StdEncoding.DecodeString(ui.OutputWriter.String())
 		require.NoError(t, err, "error decoding token")
-		require.Contains(t, string(token), "\"ServerName\":\"server.dc1.consul\"")
+		require.Contains(t, string(token), "\"ServerName\":\"server.dc1.peering.11111111-2222-3333-4444-555555555555.consul\"")
 
-		//ServerExternalAddresses
+		// ServerExternalAddresses
 		require.Contains(t, string(token), "1.2.3.4")
 		require.Contains(t, string(token), "5.6.7.8")
 
-		//Meta
+		// Meta
 		peering, _, err := client.Peerings().Read(context.Background(), "bar", &api.QueryOptions{})
 		require.NoError(t, err)
 
@@ -136,6 +136,6 @@ func TestGenerateCommand(t *testing.T) {
 
 		token, err := base64.StdEncoding.DecodeString(outputRes.PeeringToken)
 		require.NoError(t, err, "error decoding token")
-		require.Contains(t, string(token), "\"ServerName\":\"server.dc1.consul\"")
+		require.Contains(t, string(token), "\"ServerName\":\"server.dc1.peering.11111111-2222-3333-4444-555555555555.consul\"")
 	})
 }
diff --git a/sdk/testutil/server.go b/sdk/testutil/server.go
index a657919adc..928b84299b 100644
--- a/sdk/testutil/server.go
+++ b/sdk/testutil/server.go
@@ -52,6 +52,7 @@ type TestPortConfig struct {
 	SerfWan      int `json:"serf_wan,omitempty"`
 	Server       int `json:"server,omitempty"`
 	GRPC         int `json:"grpc,omitempty"`
+	GRPCTLS      int `json:"grpc_tls,omitempty"`
 	ProxyMinPort int `json:"proxy_min_port,omitempty"`
 	ProxyMaxPort int `json:"proxy_max_port,omitempty"`
 }
@@ -156,7 +157,7 @@ func defaultServerConfig(t TestingTB) *TestServerConfig {
 		panic(err)
 	}
 
-	ports := freeport.GetN(t, 7)
+	ports := freeport.GetN(t, 8)
 
 	logBuffer := NewLogBuffer(t)
 
@@ -180,6 +181,7 @@ func defaultServerConfig(t TestingTB) *TestServerConfig {
 			SerfWan: ports[4],
 			Server:  ports[5],
 			GRPC:    ports[6],
+			GRPCTLS: ports[7],
 		},
 		ReadyTimeout:   10 * time.Second,
 		StopTimeout:    10 * time.Second,
@@ -224,11 +226,12 @@ type TestServer struct {
 	cmd    *exec.Cmd
 	Config *TestServerConfig
 
-	HTTPAddr  string
-	HTTPSAddr string
-	LANAddr   string
-	WANAddr   string
-	GRPCAddr  string
+	HTTPAddr    string
+	HTTPSAddr   string
+	LANAddr     string
+	WANAddr     string
+	GRPCAddr    string
+	GRPCTLSAddr string
 
 	HTTPClient *http.Client
 
@@ -302,11 +305,12 @@ func NewTestServerConfigT(t TestingTB, cb ServerConfigCallback) (*TestServer, er
 		Config: cfg,
 		cmd:    cmd,
 
-		HTTPAddr:  httpAddr,
-		HTTPSAddr: fmt.Sprintf("127.0.0.1:%d", cfg.Ports.HTTPS),
-		LANAddr:   fmt.Sprintf("127.0.0.1:%d", cfg.Ports.SerfLan),
-		WANAddr:   fmt.Sprintf("127.0.0.1:%d", cfg.Ports.SerfWan),
-		GRPCAddr:  fmt.Sprintf("127.0.0.1:%d", cfg.Ports.GRPC),
+		HTTPAddr:    httpAddr,
+		HTTPSAddr:   fmt.Sprintf("127.0.0.1:%d", cfg.Ports.HTTPS),
+		LANAddr:     fmt.Sprintf("127.0.0.1:%d", cfg.Ports.SerfLan),
+		WANAddr:     fmt.Sprintf("127.0.0.1:%d", cfg.Ports.SerfWan),
+		GRPCAddr:    fmt.Sprintf("127.0.0.1:%d", cfg.Ports.GRPC),
+		GRPCTLSAddr: fmt.Sprintf("127.0.0.1:%d", cfg.Ports.GRPCTLS),
 
 		HTTPClient: client,
 
diff --git a/test/integration/connect/envoy/consul-base-cfg/base.hcl b/test/integration/connect/envoy/consul-base-cfg/base.hcl
index 241261c1f8..884117c5ce 100644
--- a/test/integration/connect/envoy/consul-base-cfg/base.hcl
+++ b/test/integration/connect/envoy/consul-base-cfg/base.hcl
@@ -1,2 +1,2 @@
 primary_datacenter = "primary"
-log_level          = "trace"
+log_level          = "trace"
\ No newline at end of file
diff --git a/test/integration/connect/envoy/consul-base-cfg/peering_server.hcl b/test/integration/connect/envoy/consul-base-cfg/peering_server.hcl
new file mode 100644
index 0000000000..ccbba6939c
--- /dev/null
+++ b/test/integration/connect/envoy/consul-base-cfg/peering_server.hcl
@@ -0,0 +1,6 @@
+ports {
+    grpc_tls = 8503
+}
+connect {
+    enabled = true
+}
\ No newline at end of file
diff --git a/test/integration/connect/envoy/run-tests.sh b/test/integration/connect/envoy/run-tests.sh
index 7ea41527e5..d32092e7a9 100755
--- a/test/integration/connect/envoy/run-tests.sh
+++ b/test/integration/connect/envoy/run-tests.sh
@@ -104,6 +104,13 @@ function init_workdir {
     mv workdir/${CLUSTER}/consul/server.hcl workdir/${CLUSTER}/consul-server/server.hcl
   fi
 
+  if test -f "workdir/${CLUSTER}/consul/peering_server.hcl" -a $REQUIRE_PEERS = "1"
+  then
+    mv workdir/${CLUSTER}/consul/peering_server.hcl workdir/${CLUSTER}/consul-server/peering_server.hcl
+  else
+    rm workdir/${CLUSTER}/consul/peering_server.hcl
+  fi
+
   # copy the ca-certs for SDS so we can verify the right ones are served
   mkdir -p workdir/test-sds-server/certs
   cp test-sds-server/certs/ca-root.crt workdir/test-sds-server/certs/ca-root.crt
@@ -216,11 +223,6 @@ function start_consul {
     docker_kill_rm consul-${DC}-server
     docker_kill_rm consul-${DC}
 
-    server_grpc_port="-1"
-    if is_set $REQUIRE_PEERS; then
-      server_grpc_port="8502"
-    fi
-
     docker run -d --name envoy_consul-${DC}-server_1 \
       --net=envoy-tests \
       $WORKDIR_SNIPPET \
@@ -231,7 +233,6 @@ function start_consul {
       agent -dev -datacenter "${DC}" \
       -config-dir "/workdir/${DC}/consul" \
       -config-dir "/workdir/${DC}/consul-server" \
-      -grpc-port $server_grpc_port \
       -client "0.0.0.0" \
       -bind "0.0.0.0" >/dev/null