diff --git a/agent/agent.go b/agent/agent.go
index 76fd923d4a..6a2a6fea04 100644
--- a/agent/agent.go
+++ b/agent/agent.go
@@ -797,18 +797,7 @@ func (a *Agent) listenHTTP() ([]apiServer, error) {
 				httpServer.ConnState = connLimitFn
 			}
 
-			servers = append(servers, apiServer{
-				Protocol: proto,
-				Addr:     l.Addr(),
-				Shutdown: httpServer.Shutdown,
-				Run: func() error {
-					err := httpServer.Serve(l)
-					if err == nil || err == http.ErrServerClosed {
-						return nil
-					}
-					return fmt.Errorf("%s server %s failed: %w", proto, l.Addr(), err)
-				},
-			})
+			servers = append(servers, newAPIServerHTTP(proto, l, httpServer))
 		}
 		return nil
 	}
diff --git a/agent/agent_test.go b/agent/agent_test.go
index a31a207c19..8d7d418ab0 100644
--- a/agent/agent_test.go
+++ b/agent/agent_test.go
@@ -13,6 +13,7 @@ import (
 	"net"
 	"net/http"
 	"net/http/httptest"
+	"net/url"
 	"os"
 	"path/filepath"
 	"strconv"
@@ -23,12 +24,23 @@ import (
 
 	"github.com/golang/protobuf/jsonpb"
 	"github.com/google/tcpproxy"
+	"github.com/hashicorp/go-hclog"
+	"github.com/hashicorp/serf/coordinate"
+	"github.com/hashicorp/serf/serf"
+	"github.com/stretchr/testify/assert"
+	"github.com/stretchr/testify/require"
+	"golang.org/x/sync/errgroup"
+	"golang.org/x/time/rate"
+	"gopkg.in/square/go-jose.v2/jwt"
+
 	"github.com/hashicorp/consul/agent/cache"
 	cachetype "github.com/hashicorp/consul/agent/cache-types"
 	"github.com/hashicorp/consul/agent/checks"
 	"github.com/hashicorp/consul/agent/config"
 	"github.com/hashicorp/consul/agent/connect"
+	"github.com/hashicorp/consul/agent/consul"
 	"github.com/hashicorp/consul/agent/structs"
+	"github.com/hashicorp/consul/agent/token"
 	"github.com/hashicorp/consul/api"
 	"github.com/hashicorp/consul/internal/go-sso/oidcauth/oidcauthtest"
 	"github.com/hashicorp/consul/ipaddr"
@@ -38,13 +50,8 @@ import (
 	"github.com/hashicorp/consul/sdk/testutil"
 	"github.com/hashicorp/consul/sdk/testutil/retry"
 	"github.com/hashicorp/consul/testrpc"
+	"github.com/hashicorp/consul/tlsutil"
 	"github.com/hashicorp/consul/types"
-	"github.com/hashicorp/serf/coordinate"
-	"github.com/hashicorp/serf/serf"
-	"github.com/stretchr/testify/assert"
-	"github.com/stretchr/testify/require"
-	"golang.org/x/time/rate"
-	"gopkg.in/square/go-jose.v2/jwt"
 )
 
 func getService(a *TestAgent, id string) *structs.NodeService {
@@ -4705,3 +4712,64 @@ func TestSharedRPCRouter(t *testing.T) {
 	require.NotNil(t, mgr)
 	require.NotNil(t, server)
 }
+
+func TestAgent_ListenHTTP_MultipleAddresses(t *testing.T) {
+	caConfig := tlsutil.Config{}
+	tlsConf, err := tlsutil.NewConfigurator(caConfig, hclog.New(nil))
+	require.NoError(t, err)
+	bd := BaseDeps{
+		Deps: consul.Deps{
+			Logger:          hclog.NewInterceptLogger(nil),
+			Tokens:          new(token.Store),
+			TLSConfigurator: tlsConf,
+		},
+		RuntimeConfig: &config.RuntimeConfig{
+			HTTPAddrs: []net.Addr{
+				&net.TCPAddr{IP: net.ParseIP("127.0.0.1")},
+				&net.TCPAddr{IP: net.ParseIP("127.0.0.1")},
+			},
+		},
+		Cache: cache.New(cache.Options{}),
+	}
+	agent, err := New(bd)
+	require.NoError(t, err)
+
+	srvs, err := agent.listenHTTP()
+	require.NoError(t, err)
+	defer func() {
+		ctx := context.Background()
+		for _, srv := range srvs {
+			srv.Shutdown(ctx)
+		}
+	}()
+
+	ctx, cancel := context.WithTimeout(context.Background(), 2*time.Second)
+	t.Cleanup(cancel)
+
+	g := new(errgroup.Group)
+	for _, s := range srvs {
+		g.Go(s.Run)
+	}
+
+	require.Len(t, srvs, 2)
+	require.Len(t, uniqueAddrs(srvs), 2)
+
+	client := &http.Client{}
+	for _, s := range srvs {
+		u := url.URL{Scheme: s.Protocol, Host: s.Addr.String()}
+		req, err := http.NewRequest(http.MethodGet, u.String(), nil)
+		require.NoError(t, err)
+
+		resp, err := client.Do(req.WithContext(ctx))
+		require.NoError(t, err)
+		require.Equal(t, 200, resp.StatusCode)
+	}
+}
+
+func uniqueAddrs(srvs []apiServer) map[string]struct{} {
+	result := make(map[string]struct{}, len(srvs))
+	for _, s := range srvs {
+		result[s.Addr.String()] = struct{}{}
+	}
+	return result
+}
diff --git a/agent/apiserver.go b/agent/apiserver.go
index 27087829a6..044bf60412 100644
--- a/agent/apiserver.go
+++ b/agent/apiserver.go
@@ -2,7 +2,9 @@ package agent
 
 import (
 	"context"
+	"fmt"
 	"net"
+	"net/http"
 	"sync"
 	"time"
 
@@ -92,3 +94,18 @@ func (s *apiServers) Shutdown(ctx context.Context) {
 func (s *apiServers) WaitForShutdown() error {
 	return s.group.Wait()
 }
+
+func newAPIServerHTTP(proto string, l net.Listener, httpServer *http.Server) apiServer {
+	return apiServer{
+		Protocol: proto,
+		Addr:     l.Addr(),
+		Shutdown: httpServer.Shutdown,
+		Run: func() error {
+			err := httpServer.Serve(l)
+			if err == nil || err == http.ErrServerClosed {
+				return nil
+			}
+			return fmt.Errorf("%s server %s failed: %w", proto, l.Addr(), err)
+		},
+	}
+}