diff --git a/src/gateway/auth.test.ts b/src/gateway/auth.test.ts
index 6cdc645f7..1d96886fc 100644
--- a/src/gateway/auth.test.ts
+++ b/src/gateway/auth.test.ts
@@ -1,6 +1,11 @@
 import { describe, expect, it, vi } from "vitest";
 import type { AuthRateLimiter } from "./auth-rate-limit.js";
-import { authorizeGatewayConnect, resolveGatewayAuth } from "./auth.js";
+import {
+  authorizeGatewayConnect,
+  authorizeHttpGatewayConnect,
+  authorizeWsControlUiGatewayConnect,
+  resolveGatewayAuth,
+} from "./auth.js";
 
 function createLimiterSpy(): AuthRateLimiter & {
   check: ReturnType<typeof vi.fn>;
@@ -215,7 +220,7 @@ describe("gateway auth", () => {
       auth: { mode: "token", token: "secret", allowTailscale: true },
       connectAuth: null,
       tailscaleWhois: async () => ({ login: "peter", name: "Peter" }),
-      allowTailscaleHeaderAuth: true,
+      authSurface: "ws-control-ui",
       req: {
         socket: { remoteAddress: "127.0.0.1" },
         headers: {
@@ -234,6 +239,49 @@ describe("gateway auth", () => {
     expect(res.user).toBe("peter");
   });
 
+  it("keeps tailscale header auth disabled on HTTP auth wrapper", async () => {
+    const res = await authorizeHttpGatewayConnect({
+      auth: { mode: "token", token: "secret", allowTailscale: true },
+      connectAuth: null,
+      tailscaleWhois: async () => ({ login: "peter", name: "Peter" }),
+      req: {
+        socket: { remoteAddress: "127.0.0.1" },
+        headers: {
+          host: "gateway.local",
+          "x-forwarded-for": "100.64.0.1",
+          "x-forwarded-proto": "https",
+          "x-forwarded-host": "ai-hub.bone-egret.ts.net",
+          "tailscale-user-login": "peter",
+          "tailscale-user-name": "Peter",
+        },
+      } as never,
+    });
+    expect(res.ok).toBe(false);
+    expect(res.reason).toBe("token_missing");
+  });
+
+  it("enables tailscale header auth on ws control-ui auth wrapper", async () => {
+    const res = await authorizeWsControlUiGatewayConnect({
+      auth: { mode: "token", token: "secret", allowTailscale: true },
+      connectAuth: null,
+      tailscaleWhois: async () => ({ login: "peter", name: "Peter" }),
+      req: {
+        socket: { remoteAddress: "127.0.0.1" },
+        headers: {
+          host: "gateway.local",
+          "x-forwarded-for": "100.64.0.1",
+          "x-forwarded-proto": "https",
+          "x-forwarded-host": "ai-hub.bone-egret.ts.net",
+          "tailscale-user-login": "peter",
+          "tailscale-user-name": "Peter",
+        },
+      } as never,
+    });
+    expect(res.ok).toBe(true);
+    expect(res.method).toBe("tailscale");
+    expect(res.user).toBe("peter");
+  });
+
   it("uses proxy-aware request client IP by default for rate-limit checks", async () => {
     const limiter = createLimiterSpy();
     const res = await authorizeGatewayConnect({
diff --git a/src/gateway/auth.ts b/src/gateway/auth.ts
index 76236dc2e..14c05a817 100644
--- a/src/gateway/auth.ts
+++ b/src/gateway/auth.ts
@@ -52,6 +52,27 @@ type ConnectAuth = {
   password?: string;
 };
 
+export type GatewayAuthSurface = "http" | "ws-control-ui";
+
+export type AuthorizeGatewayConnectParams = {
+  auth: ResolvedGatewayAuth;
+  connectAuth?: ConnectAuth | null;
+  req?: IncomingMessage;
+  trustedProxies?: string[];
+  tailscaleWhois?: TailscaleWhoisLookup;
+  /**
+   * Explicit auth surface. HTTP keeps Tailscale forwarded-header auth disabled.
+   * WS Control UI enables it intentionally for tokenless trusted-host login.
+   */
+  authSurface?: GatewayAuthSurface;
+  /** Optional rate limiter instance; when provided, failed attempts are tracked per IP. */
+  rateLimiter?: AuthRateLimiter;
+  /** Client IP used for rate-limit tracking. Falls back to proxy-aware request IP resolution. */
+  clientIp?: string;
+  /** Optional limiter scope; defaults to shared-secret auth scope. */
+  rateLimitScope?: string;
+};
+
 type TailscaleUser = {
   login: string;
   name: string;
@@ -319,27 +340,17 @@ function authorizeTrustedProxy(params: {
   return { user };
 }
 
-export async function authorizeGatewayConnect(params: {
-  auth: ResolvedGatewayAuth;
-  connectAuth?: ConnectAuth | null;
-  req?: IncomingMessage;
-  trustedProxies?: string[];
-  tailscaleWhois?: TailscaleWhoisLookup;
-  /**
-   * Opt-in for accepting Tailscale Serve identity headers as primary auth.
-   * Default is disabled for HTTP surfaces; WS connect enables this explicitly.
-   */
-  allowTailscaleHeaderAuth?: boolean;
-  /** Optional rate limiter instance; when provided, failed attempts are tracked per IP. */
-  rateLimiter?: AuthRateLimiter;
-  /** Client IP used for rate-limit tracking. Falls back to proxy-aware request IP resolution. */
-  clientIp?: string;
-  /** Optional limiter scope; defaults to shared-secret auth scope. */
-  rateLimitScope?: string;
-}): Promise<GatewayAuthResult> {
+function shouldAllowTailscaleHeaderAuth(authSurface: GatewayAuthSurface): boolean {
+  return authSurface === "ws-control-ui";
+}
+
+export async function authorizeGatewayConnect(
+  params: AuthorizeGatewayConnectParams,
+): Promise<GatewayAuthResult> {
   const { auth, connectAuth, req, trustedProxies } = params;
   const tailscaleWhois = params.tailscaleWhois ?? readTailscaleWhoisIdentity;
-  const allowTailscaleHeaderAuth = params.allowTailscaleHeaderAuth === true;
+  const authSurface = params.authSurface ?? "http";
+  const allowTailscaleHeaderAuth = shouldAllowTailscaleHeaderAuth(authSurface);
   const localDirect = isLocalDirectRequest(req, trustedProxies);
 
   if (auth.mode === "trusted-proxy") {
@@ -433,3 +444,21 @@ export async function authorizeGatewayConnect(params: {
   limiter?.recordFailure(ip, rateLimitScope);
   return { ok: false, reason: "unauthorized" };
 }
+
+export async function authorizeHttpGatewayConnect(
+  params: Omit<AuthorizeGatewayConnectParams, "authSurface">,
+): Promise<GatewayAuthResult> {
+  return authorizeGatewayConnect({
+    ...params,
+    authSurface: "http",
+  });
+}
+
+export async function authorizeWsControlUiGatewayConnect(
+  params: Omit<AuthorizeGatewayConnectParams, "authSurface">,
+): Promise<GatewayAuthResult> {
+  return authorizeGatewayConnect({
+    ...params,
+    authSurface: "ws-control-ui",
+  });
+}
diff --git a/src/gateway/http-auth-helpers.test.ts b/src/gateway/http-auth-helpers.test.ts
index 22ceb975d..aa3d83d5b 100644
--- a/src/gateway/http-auth-helpers.test.ts
+++ b/src/gateway/http-auth-helpers.test.ts
@@ -4,7 +4,7 @@ import type { ResolvedGatewayAuth } from "./auth.js";
 import { authorizeGatewayBearerRequestOrReply } from "./http-auth-helpers.js";
 
 vi.mock("./auth.js", () => ({
-  authorizeGatewayConnect: vi.fn(),
+  authorizeHttpGatewayConnect: vi.fn(),
 }));
 
 vi.mock("./http-common.js", () => ({
@@ -15,7 +15,7 @@ vi.mock("./http-utils.js", () => ({
   getBearerToken: vi.fn(),
 }));
 
-const { authorizeGatewayConnect } = await import("./auth.js");
+const { authorizeHttpGatewayConnect } = await import("./auth.js");
 const { sendGatewayAuthFailure } = await import("./http-common.js");
 const { getBearerToken } = await import("./http-utils.js");
 
@@ -26,7 +26,7 @@ describe("authorizeGatewayBearerRequestOrReply", () => {
 
   it("disables tailscale header auth for HTTP bearer checks", async () => {
     vi.mocked(getBearerToken).mockReturnValue(undefined);
-    vi.mocked(authorizeGatewayConnect).mockResolvedValue({
+    vi.mocked(authorizeHttpGatewayConnect).mockResolvedValue({
       ok: false,
       reason: "token_missing",
     });
@@ -43,9 +43,8 @@ describe("authorizeGatewayBearerRequestOrReply", () => {
     });
 
     expect(ok).toBe(false);
-    expect(vi.mocked(authorizeGatewayConnect)).toHaveBeenCalledWith(
+    expect(vi.mocked(authorizeHttpGatewayConnect)).toHaveBeenCalledWith(
       expect.objectContaining({
-        allowTailscaleHeaderAuth: false,
         connectAuth: null,
       }),
     );
@@ -54,7 +53,7 @@ describe("authorizeGatewayBearerRequestOrReply", () => {
 
   it("forwards bearer token and returns true on successful auth", async () => {
     vi.mocked(getBearerToken).mockReturnValue("abc");
-    vi.mocked(authorizeGatewayConnect).mockResolvedValue({ ok: true, method: "token" });
+    vi.mocked(authorizeHttpGatewayConnect).mockResolvedValue({ ok: true, method: "token" });
 
     const ok = await authorizeGatewayBearerRequestOrReply({
       req: {} as IncomingMessage,
@@ -68,9 +67,8 @@ describe("authorizeGatewayBearerRequestOrReply", () => {
     });
 
     expect(ok).toBe(true);
-    expect(vi.mocked(authorizeGatewayConnect)).toHaveBeenCalledWith(
+    expect(vi.mocked(authorizeHttpGatewayConnect)).toHaveBeenCalledWith(
       expect.objectContaining({
-        allowTailscaleHeaderAuth: false,
         connectAuth: { token: "abc", password: "abc" },
       }),
     );
diff --git a/src/gateway/http-auth-helpers.ts b/src/gateway/http-auth-helpers.ts
index a7ee69eb6..36edb7c8d 100644
--- a/src/gateway/http-auth-helpers.ts
+++ b/src/gateway/http-auth-helpers.ts
@@ -1,6 +1,6 @@
 import type { IncomingMessage, ServerResponse } from "node:http";
 import type { AuthRateLimiter } from "./auth-rate-limit.js";
-import { authorizeGatewayConnect, type ResolvedGatewayAuth } from "./auth.js";
+import { authorizeHttpGatewayConnect, type ResolvedGatewayAuth } from "./auth.js";
 import { sendGatewayAuthFailure } from "./http-common.js";
 import { getBearerToken } from "./http-utils.js";
 
@@ -12,12 +12,11 @@ export async function authorizeGatewayBearerRequestOrReply(params: {
   rateLimiter?: AuthRateLimiter;
 }): Promise<boolean> {
   const token = getBearerToken(params.req);
-  const authResult = await authorizeGatewayConnect({
+  const authResult = await authorizeHttpGatewayConnect({
     auth: params.auth,
     connectAuth: token ? { token, password: token } : null,
     req: params.req,
     trustedProxies: params.trustedProxies,
-    allowTailscaleHeaderAuth: false,
     rateLimiter: params.rateLimiter,
   });
   if (!authResult.ok) {
diff --git a/src/gateway/server-http.ts b/src/gateway/server-http.ts
index 6cabb0fb4..c1c29b355 100644
--- a/src/gateway/server-http.ts
+++ b/src/gateway/server-http.ts
@@ -21,7 +21,7 @@ import { safeEqualSecret } from "../security/secret-equal.js";
 import { handleSlackHttpRequest } from "../slack/http/index.js";
 import type { AuthRateLimiter } from "./auth-rate-limit.js";
 import {
-  authorizeGatewayConnect,
+  authorizeHttpGatewayConnect,
   isLocalDirectRequest,
   type GatewayAuthResult,
   type ResolvedGatewayAuth,
@@ -150,12 +150,11 @@ async function authorizeCanvasRequest(params: {
   let lastAuthFailure: GatewayAuthResult | null = null;
   const token = getBearerToken(req);
   if (token) {
-    const authResult = await authorizeGatewayConnect({
+    const authResult = await authorizeHttpGatewayConnect({
       auth: { ...auth, allowTailscale: false },
       connectAuth: { token, password: token },
       req,
       trustedProxies,
-      allowTailscaleHeaderAuth: false,
       rateLimiter,
     });
     if (authResult.ok) {
@@ -528,12 +527,11 @@ export function createGatewayHttpServer(opts: {
         // their own auth when exposing sensitive functionality.
         if (requestPath.startsWith("/api/channels/")) {
           const token = getBearerToken(req);
-          const authResult = await authorizeGatewayConnect({
+          const authResult = await authorizeHttpGatewayConnect({
             auth: resolvedAuth,
             connectAuth: token ? { token, password: token } : null,
             req,
             trustedProxies,
-            allowTailscaleHeaderAuth: false,
             rateLimiter,
           });
           if (!authResult.ok) {
diff --git a/src/gateway/server/ws-connection/message-handler.ts b/src/gateway/server/ws-connection/message-handler.ts
index 92a3d1e5c..1be8b5778 100644
--- a/src/gateway/server/ws-connection/message-handler.ts
+++ b/src/gateway/server/ws-connection/message-handler.ts
@@ -30,7 +30,11 @@ import {
   type AuthRateLimiter,
 } from "../../auth-rate-limit.js";
 import type { GatewayAuthResult, ResolvedGatewayAuth } from "../../auth.js";
-import { authorizeGatewayConnect, isLocalDirectRequest } from "../../auth.js";
+import {
+  authorizeHttpGatewayConnect,
+  authorizeWsControlUiGatewayConnect,
+  isLocalDirectRequest,
+} from "../../auth.js";
 import {
   buildCanvasScopedHostUrl,
   CANVAS_CAPABILITY_TTL_MS,
@@ -380,12 +384,11 @@ export function attachGatewayWsMessageHandler(params: {
 
         const resolveAuthState = async () => {
           const hasDeviceTokenCandidate = Boolean(connectParams.auth?.token && device);
-          let nextAuthResult: GatewayAuthResult = await authorizeGatewayConnect({
+          let nextAuthResult: GatewayAuthResult = await authorizeWsControlUiGatewayConnect({
             auth: resolvedAuth,
             connectAuth: connectParams.auth,
             req: upgradeReq,
             trustedProxies,
-            allowTailscaleHeaderAuth: true,
             rateLimiter: hasDeviceTokenCandidate ? undefined : rateLimiter,
             clientIp,
             rateLimitScope: AUTH_RATE_LIMIT_SCOPE_SHARED_SECRET,
@@ -416,7 +419,7 @@ export function attachGatewayWsMessageHandler(params: {
           const nextAuthMethod =
             nextAuthResult.method ?? (resolvedAuth.mode === "password" ? "password" : "token");
           const sharedAuthResult = hasSharedAuth
-            ? await authorizeGatewayConnect({
+            ? await authorizeHttpGatewayConnect({
                 auth: { ...resolvedAuth, allowTailscale: false },
                 connectAuth: connectParams.auth,
                 req: upgradeReq,
diff --git a/src/gateway/tools-invoke-http.test.ts b/src/gateway/tools-invoke-http.test.ts
index eea4ebb8b..2a631f9c3 100644
--- a/src/gateway/tools-invoke-http.test.ts
+++ b/src/gateway/tools-invoke-http.test.ts
@@ -34,7 +34,7 @@ vi.mock("../config/sessions.js", () => ({
 }));
 
 vi.mock("./auth.js", () => ({
-  authorizeGatewayConnect: async () => ({ ok: true }),
+  authorizeHttpGatewayConnect: async () => ({ ok: true }),
 }));
 
 vi.mock("../logger.js", () => ({
diff --git a/src/gateway/tools-invoke-http.ts b/src/gateway/tools-invoke-http.ts
index eda5b8164..84f14457f 100644
--- a/src/gateway/tools-invoke-http.ts
+++ b/src/gateway/tools-invoke-http.ts
@@ -24,7 +24,7 @@ import { isSubagentSessionKey } from "../routing/session-key.js";
 import { DEFAULT_GATEWAY_HTTP_TOOL_DENY } from "../security/dangerous-tools.js";
 import { normalizeMessageChannel } from "../utils/message-channel.js";
 import type { AuthRateLimiter } from "./auth-rate-limit.js";
-import { authorizeGatewayConnect, type ResolvedGatewayAuth } from "./auth.js";
+import { authorizeHttpGatewayConnect, type ResolvedGatewayAuth } from "./auth.js";
 import {
   readJsonBodyOrError,
   sendGatewayAuthFailure,
@@ -146,12 +146,11 @@ export async function handleToolsInvokeHttpRequest(
 
   const cfg = loadConfig();
   const token = getBearerToken(req);
-  const authResult = await authorizeGatewayConnect({
+  const authResult = await authorizeHttpGatewayConnect({
     auth: opts.auth,
     connectAuth: token ? { token, password: token } : null,
     req,
     trustedProxies: opts.trustedProxies ?? cfg.gateway?.trustedProxies,
-    allowTailscaleHeaderAuth: false,
     rateLimiter: opts.rateLimiter,
   });
   if (!authResult.ok) {