diff --git a/lib/utils/cli.go b/lib/utils/cli.go
index 6821764c73196..2b1c7fd20412d 100644
--- a/lib/utils/cli.go
+++ b/lib/utils/cli.go
@@ -238,6 +238,51 @@ func formatCertError(err error) string {
 
 	var hostnameErr x509.HostnameError
 	if errors.As(err, &hostnameErr) {
+		// Special case for connecting to Auth via Proxy using internal cluster domain.
+		if strings.HasSuffix(hostnameErr.Host, ".teleport.cluster.local") {
+			var proxyEnvBuilder strings.Builder
+			for _, key := range []string{
+				"https_proxy", "http_proxy", "no_proxy",
+				"HTTPS_PROXY", "HTTP_PROXY", "NO_PROXY",
+			} {
+				if val, ok := os.LookupEnv(key); ok {
+					fmt.Fprintf(&proxyEnvBuilder, "    %s: %s\n", key, val)
+				}
+			}
+
+			return fmt.Sprintf(`Cannot connect to the Auth service via the Teleport Proxy.
+
+  There might be one or more network intermediaries (like a proxy or VPN) that are modifying your connection before it
+  reaches the Teleport Proxy. These intermediaries can alter how your connection is seen by the Teleport Proxy and
+  routed, leading to certificate mismatches.
+
+  To fix this, ensure that any network intermediaries are properly configured and not interfering with your connection.
+
+DEBUG INFO:
+  Host: %s
+
+  Proxy Environment Variables:
+%s
+  Server Certificate Details:
+    Subject: %s
+    Issuer: %s
+    Serial Number: %s
+    Not Before: %s
+    Not After: %s
+    DNS Names: %v
+    IP Addresses: %v`,
+				hostnameErr.Host,
+				proxyEnvBuilder.String(),
+				hostnameErr.Certificate.Subject,
+				hostnameErr.Certificate.Issuer,
+				hostnameErr.Certificate.SerialNumber,
+				hostnameErr.Certificate.NotBefore,
+				hostnameErr.Certificate.NotAfter,
+				hostnameErr.Certificate.DNSNames,
+				hostnameErr.Certificate.IPAddresses,
+			)
+		}
+
 		return fmt.Sprintf("Cannot establish https connection to %s:\n%s\n%s\n",
 			hostnameErr.Host,
 			hostnameErr.Error(),
diff --git a/lib/utils/cli_test.go b/lib/utils/cli_test.go
index 7e299c410d2e4..d9b2b04609a12 100644
--- a/lib/utils/cli_test.go
+++ b/lib/utils/cli_test.go
@@ -20,6 +20,7 @@ package utils
 
 import (
 	"crypto/x509"
+	"errors"
 	"fmt"
 	"log/slog"
 	"testing"
@@ -212,3 +213,45 @@ func TestFilterArguments(t *testing.T) {
 		require.Equal(t, tt.expected, FilterArguments(tt.args, app.Model()), fmt.Sprintf("test case %v", i))
 	}
 }
+
+// TestFormatCertError tests the formatCertError function for various x509 error types and messages.
+func TestFormatCertError(t *testing.T) {
+	t.Run("UnknownAuthorityError", func(t *testing.T) {
+		err := x509.UnknownAuthorityError{}
+		msg := formatCertError(err)
+		require.Contains(t, msg, "The proxy you are connecting to has presented a certificate signed by a")
+	})
+
+	t.Run("HostnameErrorConnectingToAuth", func(t *testing.T) {
+		cert := &x509.Certificate{Raw: []byte("dummy")}
+		err := x509.HostnameError{Certificate: cert, Host: "99999999999999999999999999999999.teleport.cluster.local"}
+		msg := formatCertError(err)
+		require.Contains(t, msg, "Cannot connect to the Auth service via the Teleport Proxy.")
+		require.Contains(t, msg, "Host: 99999999999999999999999999999999.teleport.cluster.local")
+	})
+
+	t.Run("HostnameError", func(t *testing.T) {
+		cert := &x509.Certificate{Raw: []byte("dummy")}
+		err := x509.HostnameError{Certificate: cert, Host: "example.com"}
+		msg := formatCertError(err)
+		require.Contains(t, msg, "Cannot establish https connection to example.com")
+	})
+
+	t.Run("CertificateInvalidError", func(t *testing.T) {
+		err := x509.CertificateInvalidError{Reason: x509.Expired, Cert: &x509.Certificate{}}
+		msg := formatCertError(err)
+		require.Contains(t, msg, "The certificate presented by the proxy is invalid")
+	})
+
+	t.Run("CertificateNotTrustedError", func(t *testing.T) {
+		err := errors.New("certificate is not trusted")
+		msg := formatCertError(err)
+		require.Contains(t, msg, "The proxy you are connecting to has presented a certificate signed by")
+	})
+
+	t.Run("NoMatch", func(t *testing.T) {
+		err := errors.New("some other error")
+		msg := formatCertError(err)
+		require.Empty(t, msg)
+	})
+}