diff --git a/src/cli/daemon-cli/lifecycle.test.ts b/src/cli/daemon-cli/lifecycle.test.ts
index 20ee6a69a76..266d85e0775 100644
--- a/src/cli/daemon-cli/lifecycle.test.ts
+++ b/src/cli/daemon-cli/lifecycle.test.ts
@@ -39,16 +39,17 @@ const resolveGatewayPort = vi.hoisted(() => vi.fn((_cfg?: unknown, _env?: unknow
 const findVerifiedGatewayListenerPidsOnPortSync = vi.fn<(port: number) => number[]>(() => []);
 const signalVerifiedGatewayPidSync = vi.fn<(pid: number, signal: "SIGTERM" | "SIGUSR1") => void>();
 const formatGatewayPidList = vi.fn<(pids: number[]) => string>((pids) => pids.join(", "));
-const probeGateway = vi.fn<
-  (opts: {
-    url: string;
-    auth?: { token?: string; password?: string };
-    timeoutMs: number;
-  }) => Promise<{
-    ok: boolean;
-    configSnapshot: unknown;
-  }>
->();
+const probeGateway =
+  vi.fn<
+    (opts: {
+      url: string;
+      auth?: { token?: string; password?: string };
+      timeoutMs: number;
+    }) => Promise<{
+      ok: boolean;
+      configSnapshot: unknown;
+    }>
+  >();
 const isRestartEnabled = vi.fn<(config?: { commands?: unknown }) => boolean>(() => true);
 const loadConfig = vi.hoisted(() => vi.fn(() => ({})));
 const recoverInstalledLaunchAgent = vi.hoisted(() => vi.fn());
diff --git a/src/gateway/call.ts b/src/gateway/call.ts
index 51a5d6cc4fc..ce2612b4eb8 100644
--- a/src/gateway/call.ts
+++ b/src/gateway/call.ts
@@ -406,7 +406,17 @@ function formatGatewayCloseError(
   const hint =
     code === 1006 ? "abnormal closure (no close frame)" : code === 1000 ? "normal closure" : "";
   const suffix = hint ? ` ${hint}` : "";
-  return `gateway closed (${code}${suffix}): ${reasonText}\n${connectionDetails.message}`;
+  let message = `gateway closed (${code}${suffix}): ${reasonText}\n${connectionDetails.message}`;
+  // Add troubleshooting hints for common issues
+  if (code === 1006) {
+    message +=
+      "\n\nPossible causes:" +
+      "\n- Gateway not yet ready to accept connections (retry after a moment)" +
+      "\n- TLS mismatch (connecting with ws:// to a wss:// gateway, or vice versa)" +
+      "\n- Gateway crashed or was terminated unexpectedly" +
+      "\nRun `openclaw doctor` for diagnostics.";
+  }
+  return message;
 }
 
 function formatGatewayTimeoutError(
diff --git a/src/gateway/server-http.ts b/src/gateway/server-http.ts
index 396e8b510eb..439fe864aad 100644
--- a/src/gateway/server-http.ts
+++ b/src/gateway/server-http.ts
@@ -1139,6 +1139,8 @@ export function attachGatewayUpgradeHandler(opts: {
   getResolvedAuth?: () => ResolvedGatewayAuth;
   /** Optional rate limiter for auth brute-force protection. */
   rateLimiter?: AuthRateLimiter;
+  /** Optional logger for error diagnostics. */
+  log?: { warn: (msg: string) => void };
 }) {
   const {
     httpServer,
@@ -1148,6 +1150,7 @@ export function attachGatewayUpgradeHandler(opts: {
     preauthConnectionBudget,
     resolvedAuth,
     rateLimiter,
+    log,
   } = opts;
   const getResolvedAuth = opts.getResolvedAuth ?? (() => resolvedAuth);
   httpServer.on("upgrade", (req, socket, head) => {
@@ -1250,7 +1253,10 @@ export function attachGatewayUpgradeHandler(opts: {
         releaseUpgradeBudget();
         throw new Error("gateway websocket upgrade failed");
       }
-    })().catch(() => {
+    })().catch((err) => {
+      const remoteAddress = (socket as { remoteAddress?: string }).remoteAddress ?? "unknown";
+      const errorMessage = err instanceof Error ? err.message : String(err);
+      log?.warn(`ws upgrade error from ${remoteAddress}: ${errorMessage}`);
       socket.destroy();
     });
   });
diff --git a/src/gateway/server-runtime-state.ts b/src/gateway/server-runtime-state.ts
index 2058636c526..b77548ed615 100644
--- a/src/gateway/server-runtime-state.ts
+++ b/src/gateway/server-runtime-state.ts
@@ -84,6 +84,7 @@ export async function createGatewayRuntimeState(params: {
   httpServer: HttpServer;
   httpServers: HttpServer[];
   httpBindHosts: string[];
+  startListening: () => Promise<void>;
   wss: WebSocketServer;
   preauthConnectionBudget: PreauthConnectionBudget;
   clients: Set<GatewayWsClient>;
@@ -168,9 +169,18 @@ export async function createGatewayRuntimeState(params: {
           "Host-header origin fallback weakens origin checks and should only be used as break-glass.",
       );
     }
+    // Create WebSocketServer first (with noServer: true) so we can attach upgrade handlers
+    // before HTTP servers start listening. This prevents a race condition where connections
+    // arrive before the upgrade handler is attached, which causes silent 1006 errors.
+    const wss = new WebSocketServer({
+      noServer: true,
+      maxPayload: MAX_PREAUTH_PAYLOAD_BYTES,
+    });
+    const preauthConnectionBudget = createPreauthConnectionBudget();
+
     const httpServers: HttpServer[] = [];
     const httpBindHosts: string[] = [];
-    for (const host of bindHosts) {
+    for (const _host of bindHosts) {
       const httpServer = createGatewayHttpServer({
         canvasHost,
         clients,
@@ -191,36 +201,9 @@ export async function createGatewayRuntimeState(params: {
         getReadiness: params.getReadiness,
         tlsOptions: params.gatewayTls?.enabled ? params.gatewayTls.tlsOptions : undefined,
       });
-      try {
-        await listenGatewayHttpServer({
-          httpServer,
-          bindHost: host,
-          port: params.port,
-        });
-        httpServers.push(httpServer);
-        httpBindHosts.push(host);
-      } catch (err) {
-        if (host === bindHosts[0]) {
-          throw err;
-        }
-        params.log.warn(
-          `gateway: failed to bind loopback alias ${host}:${params.port} (${String(err)})`,
-        );
-      }
-    }
-    const httpServer = httpServers[0];
-    if (!httpServer) {
-      throw new Error("Gateway HTTP server failed to start");
-    }
-
-    const wss = new WebSocketServer({
-      noServer: true,
-      maxPayload: MAX_PREAUTH_PAYLOAD_BYTES,
-    });
-    const preauthConnectionBudget = createPreauthConnectionBudget();
-    for (const server of httpServers) {
+      // Attach upgrade handler BEFORE listening to prevent race condition
       attachGatewayUpgradeHandler({
-        httpServer: server,
+        httpServer,
         wss,
         canvasHost,
         clients,
@@ -228,9 +211,53 @@ export async function createGatewayRuntimeState(params: {
         resolvedAuth: params.resolvedAuth,
         getResolvedAuth: params.getResolvedAuth,
         rateLimiter: params.rateLimiter,
+        log: params.log,
       });
+      httpServers.push(httpServer);
     }
-
+    const httpServer = httpServers[0];
+    if (!httpServer) {
+      throw new Error("Gateway HTTP server failed to start");
+    }
+    let startListeningPromise: Promise<void> | null = null;
+    const startListening = async (): Promise<void> => {
+      if (startListeningPromise) {
+        await startListeningPromise;
+        return;
+      }
+      startListeningPromise = (async () => {
+        for (const [index, host] of bindHosts.entries()) {
+          const server = httpServers[index];
+          if (!server) {
+            throw new Error(`Missing gateway HTTP server for bind host ${host}`);
+          }
+          try {
+            await listenGatewayHttpServer({
+              httpServer: server,
+              bindHost: host,
+              port: params.port,
+            });
+            httpBindHosts.push(host);
+          } catch (err) {
+            if (host === bindHosts[0]) {
+              throw err;
+            }
+            params.log.warn(
+              `gateway: failed to bind loopback alias ${host}:${params.port} (${String(err)})`,
+            );
+          }
+        }
+        if (httpBindHosts.length === 0) {
+          throw new Error("Gateway HTTP server failed to start");
+        }
+      })();
+      try {
+        await startListeningPromise;
+      } catch (err) {
+        startListeningPromise = null;
+        throw err;
+      }
+    };
     const agentRunSeq = new Map<string, number>();
     const dedupe = new Map<string, DedupeEntry>();
     const chatRunState = createChatRunState();
@@ -257,6 +284,7 @@ export async function createGatewayRuntimeState(params: {
       httpServer,
       httpServers,
       httpBindHosts,
+      startListening,
       wss,
       preauthConnectionBudget,
       clients,