diff --git a/api/client/errors.go b/api/client/errors.go
new file mode 100644
index 0000000000000..69ee906467885
--- /dev/null
+++ b/api/client/errors.go
@@ -0,0 +1,21 @@
+// Copyright 2024 Gravitational, Inc.
+//
+// Licensed under the Apache License, Version 2.0 (the "License");
+// you may not use this file except in compliance with the License.
+// You may obtain a copy of the License at
+//
+//      http://www.apache.org/licenses/LICENSE-2.0
+//
+// Unless required by applicable law or agreed to in writing, software
+// distributed under the License is distributed on an "AS IS" BASIS,
+// WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+// See the License for the specific language governing permissions and
+// limitations under the License.
+
+package client
+
+import "github.com/gravitational/trace"
+
+// ErrClientCredentialsHaveExpired means that the credentials expired on
+// the server-side and the user should relogin.
+var ErrClientCredentialsHaveExpired = &trace.AccessDeniedError{Message: "access denied: client credentials have expired, please relogin."}
diff --git a/lib/auth/auth_with_roles.go b/lib/auth/auth_with_roles.go
index dcf0dad828e6e..294d1bf33b7d9 100644
--- a/lib/auth/auth_with_roles.go
+++ b/lib/auth/auth_with_roles.go
@@ -2898,7 +2898,7 @@ func (a *ServerWithRoles) generateUserCerts(ctx context.Context, req proto.UserC
 			return nil, trace.AccessDenied("access denied")
 		}
 		if req.Expires.Before(a.authServer.GetClock().Now()) {
-			return nil, trace.AccessDenied("access denied: client credentials have expired, please relogin.")
+			return nil, trace.Wrap(client.ErrClientCredentialsHaveExpired)
 		}
 
 		if identity.Renewable || isRoleImpersonation(req) {
diff --git a/lib/client/api.go b/lib/client/api.go
index 2d050e40c17aa..373853aa06304 100644
--- a/lib/client/api.go
+++ b/lib/client/api.go
@@ -679,7 +679,17 @@ func IsErrorResolvableWithRelogin(err error) bool {
 	// https://github.com/gravitational/teleport/pull/30578.
 	var remoteErr *interceptors.RemoteError
 	if errors.As(err, &remoteErr) {
-		return false
+		// Exception for the two "retryable" errors that come from RPCs.
+		//
+		// Since Connect no longer checks the user cert before making an RPC,
+		// it has to be able to properly recognize "expired certs" errors
+		// that come from the server (to show a re-login dialog).
+		//
+		// TODO(gzdunek): These manual checks should be replaced with retryable
+		// errors returned explicitly, as described below by codingllama.
+		isClientCredentialsHaveExpired := errors.Is(err, client.ErrClientCredentialsHaveExpired)
+		isTLSExpiredCertificate := strings.Contains(err.Error(), "tls: expired certificate")
+		return isClientCredentialsHaveExpired || isTLSExpiredCertificate
 	}
 
 	return keys.IsPrivateKeyPolicyError(err) ||