diff --git a/.changelog/16266.txt b/.changelog/16266.txt
new file mode 100644
index 0000000000..72dbc39800
--- /dev/null
+++ b/.changelog/16266.txt
@@ -0,0 +1,3 @@
+```release-note:improvement
+ca: support Vault agent auto-auth config for Vault CA provider using JWT authentication.
+```
diff --git a/agent/connect/ca/provider_vault.go b/agent/connect/ca/provider_vault.go
index 7954e7ea03..1244c79455 100644
--- a/agent/connect/ca/provider_vault.go
+++ b/agent/connect/ca/provider_vault.go
@@ -935,6 +935,8 @@ func configureVaultAuthMethod(authMethod *structs.VaultAuthMethod) (VaultAuthent
 		return NewAzureAuthClient(authMethod)
 	case VaultAuthMethodTypeGCP:
 		return NewGCPAuthClient(authMethod)
+	case VaultAuthMethodTypeJWT:
+		return NewJwtAuthClient(authMethod)
 	case VaultAuthMethodTypeKubernetes:
 		// For the Kubernetes Auth method, we will try to read the JWT token
 		// from the default service account file location if jwt was not provided.
@@ -972,7 +974,6 @@ func configureVaultAuthMethod(authMethod *structs.VaultAuthMethod) (VaultAuthent
 		VaultAuthMethodTypeAppRole,
 		VaultAuthMethodTypeCloudFoundry,
 		VaultAuthMethodTypeGitHub,
-		VaultAuthMethodTypeJWT,
 		VaultAuthMethodTypeKerberos,
 		VaultAuthMethodTypeTLS:
 		return NewVaultAPIAuthClient(authMethod, loginPath), nil
diff --git a/agent/connect/ca/provider_vault_auth_jwt.go b/agent/connect/ca/provider_vault_auth_jwt.go
new file mode 100644
index 0000000000..e95481b55c
--- /dev/null
+++ b/agent/connect/ca/provider_vault_auth_jwt.go
@@ -0,0 +1,50 @@
+package ca
+
+import (
+	"fmt"
+	"os"
+	"strings"
+
+	"github.com/hashicorp/consul/agent/structs"
+)
+
+func NewJwtAuthClient(authMethod *structs.VaultAuthMethod) (*VaultAuthClient, error) {
+	params := authMethod.Params
+
+	role, ok := params["role"].(string)
+	if !ok || strings.TrimSpace(role) == "" {
+		return nil, fmt.Errorf("missing 'role' value")
+	}
+
+	authClient := NewVaultAPIAuthClient(authMethod, "")
+	if legacyCheck(params, "jwt") {
+		return authClient, nil
+	}
+
+	// The path is required for the auto-auth config, but this auth provider
+	// seems to be used for jwt based auth by directly passing the jwt token.
+	// So we only require the token file path if the token string isn't
+	// present.
+	tokenPath, ok := params["path"].(string)
+	if !ok || strings.TrimSpace(tokenPath) == "" {
+		return nil, fmt.Errorf("missing 'path' value")
+	}
+	authClient.LoginDataGen = JwtLoginDataGen
+	return authClient, nil
+}
+
+func JwtLoginDataGen(authMethod *structs.VaultAuthMethod) (map[string]any, error) {
+	params := authMethod.Params
+	role := params["role"].(string)
+
+	tokenPath := params["path"].(string)
+	rawToken, err := os.ReadFile(tokenPath)
+	if err != nil {
+		return nil, err
+	}
+
+	return map[string]any{
+		"role": role,
+		"jwt":  strings.TrimSpace(string(rawToken)),
+	}, nil
+}
diff --git a/agent/connect/ca/provider_vault_auth_test.go b/agent/connect/ca/provider_vault_auth_test.go
index 2b0a04a46f..7a38729307 100644
--- a/agent/connect/ca/provider_vault_auth_test.go
+++ b/agent/connect/ca/provider_vault_auth_test.go
@@ -428,3 +428,77 @@ func TestVaultCAProvider_AzureAuthClient(t *testing.T) {
 		})
 	}
 }
+
+func TestVaultCAProvider_JwtAuthClient(t *testing.T) {
+	tokenF, err := os.CreateTemp("", "token-path")
+	require.NoError(t, err)
+	defer func() { os.Remove(tokenF.Name()) }()
+	_, err = tokenF.WriteString("test-token")
+	require.NoError(t, err)
+	err = tokenF.Close()
+	require.NoError(t, err)
+
+	cases := map[string]struct {
+		authMethod *structs.VaultAuthMethod
+		expData    map[string]any
+		expErr     error
+	}{
+		"base-case": {
+			authMethod: &structs.VaultAuthMethod{
+				Type: "jwt",
+				Params: map[string]any{
+					"role": "test-role",
+					"path": tokenF.Name(),
+				},
+			},
+			expData: map[string]any{
+				"role": "test-role",
+				"jwt":  "test-token",
+			},
+		},
+		"no-role": {
+			authMethod: &structs.VaultAuthMethod{
+				Type:   "jwt",
+				Params: map[string]any{},
+			},
+			expErr: fmt.Errorf("missing 'role' value"),
+		},
+		"no-path": {
+			authMethod: &structs.VaultAuthMethod{
+				Type: "jwt",
+				Params: map[string]any{
+					"role": "test-role",
+				},
+			},
+			expErr: fmt.Errorf("missing 'path' value"),
+		},
+		"no-path-but-jwt": {
+			authMethod: &structs.VaultAuthMethod{
+				Type: "jwt",
+				Params: map[string]any{
+					"role": "test-role",
+					"jwt":  "test-jwt",
+				},
+			},
+			expData: map[string]any{
+				"role": "test-role",
+				"jwt":  "test-jwt",
+			},
+		},
+	}
+	for name, c := range cases {
+		t.Run(name, func(t *testing.T) {
+			auth, err := NewJwtAuthClient(c.authMethod)
+			if c.expErr != nil {
+				require.EqualError(t, c.expErr, err.Error())
+				return
+			}
+			require.NoError(t, err)
+			if auth.LoginDataGen != nil {
+				data, err := auth.LoginDataGen(c.authMethod)
+				require.NoError(t, err)
+				require.Equal(t, c.expData, data)
+			}
+		})
+	}
+}
diff --git a/agent/connect/ca/provider_vault_test.go b/agent/connect/ca/provider_vault_test.go
index 173d2c5549..a834c71877 100644
--- a/agent/connect/ca/provider_vault_test.go
+++ b/agent/connect/ca/provider_vault_test.go
@@ -111,7 +111,7 @@ func TestVaultCAProvider_configureVaultAuthMethod(t *testing.T) {
 		"cf":          {expLoginPath: "auth/cf/login"},
 		"github":      {expLoginPath: "auth/github/login"},
 		"gcp":         {expLoginPath: "auth/gcp/login", params: map[string]interface{}{"type": "iam", "role": "test-role"}},
-		"jwt":         {expLoginPath: "auth/jwt/login"},
+		"jwt":         {expLoginPath: "auth/jwt/login", params: map[string]any{"role": "test-role", "path": "test-path"}, hasLDG: true},
 		"kerberos":    {expLoginPath: "auth/kerberos/login"},
 		"kubernetes":  {expLoginPath: "auth/kubernetes/login", params: map[string]interface{}{"jwt": "fake"}},
 		"ldap":        {expLoginPath: "auth/ldap/login/foo", params: map[string]interface{}{"username": "foo"}},