diff --git a/src/agent_manager/api/static/widget.js b/src/agent_manager/api/static/widget.js
index e9614007..9ad731af 100644
--- a/src/agent_manager/api/static/widget.js
+++ b/src/agent_manager/api/static/widget.js
@@ -52299,6 +52299,8 @@ var TokenSource = class {
     /** Bumped by `reset()` so a resolution already in flight, once it lands, can
      *  tell it is answering a question nobody is asking anymore. */
     this.generation = 0;
+    /** Avoid repeating unauthenticated claim attempts for the same pass in cookie mode. */
+    this.lastClaimAttemptPass = null;
     this.tokenUrl = options.tokenUrl ?? "";
     this.provider = options.provider ?? null;
     this.storage = options.storage ?? localStorage;
@@ -52307,7 +52309,9 @@ var TokenSource = class {
     });
   }
   async current() {
-    if (!this.cached) await this.resolve(() => this.storedPass());
+    if (!this.cached || this.isCookieMode() && this.storedPass() !== null) {
+      await this.resolve(() => this.storedPass());
+    }
     return this.cached;
   }
   /** After a 401: whatever we sent is no good, so get another. */
@@ -52344,23 +52348,38 @@ var TokenSource = class {
     })());
     return this.pending;
   }
+  isCookieMode() {
+    return !this.tokenUrl && !this.provider;
+  }
   /** A host token, plus the one-time hand-off of whatever this browser chatted
    *  about before signing in. */
   async hostToken() {
     const token = await this.fromHost();
-    if (token) await this.claimVisitorHistory(token);
+    if (token || this.isCookieMode() && this.storedPass()) {
+      await this.claimVisitorHistory(token);
+    }
     return token;
   }
   async claimVisitorHistory(hostToken) {
     const pass = this.storedPass();
     if (!pass) return;
     try {
+      const headers = { "Content-Type": "application/json" };
+      if (hostToken) headers.Authorization = `Bearer ${hostToken}`;
       const response = await fetch(`${this.endpoint}${LINK_ENDPOINT}`, {
         method: "POST",
-        headers: { "Content-Type": "application/json", Authorization: `Bearer ${hostToken}` },
+        headers,
+        credentials: "include",
         body: JSON.stringify({ anonymous_token: pass })
       });
-      if (response.status < 500) this.clearPass();
+      if (response.ok) {
+        const data = await response.json().catch(() => null);
+        if (hostToken !== null || (data?.conversations_moved ?? 0) > 0) {
+          this.clearPass();
+        }
+      } else if (hostToken !== null && response.status >= 400 && response.status < 500 && response.status !== 401) {
+        this.clearPass();
+      }
     } catch {
     }
   }
diff --git a/src/agent_manager/api/static/widget.test.mjs b/src/agent_manager/api/static/widget.test.mjs
index 2feb6279..d8b87794 100644
--- a/src/agent_manager/api/static/widget.test.mjs
+++ b/src/agent_manager/api/static/widget.test.mjs
@@ -747,6 +747,44 @@ assert.equal(mintedPass, false, "never asks for a visitor pass");
   );
 }
 
+// In cookie mode (host_token), a visitor chats anonymously, then signs in via cookie in the same SPA.
+// Calling client methods re-evaluates identity, claims history via /auth/link, and sends requests with cookie.
+{
+  resetPage();
+  localStorage.setItem(visitorPassKey("https://api.example"), "old-cookie-pass");
+  let loggedInViaCookie = false;
+  const calls = [];
+  globalThis.fetch = async (url, options = {}) => {
+    calls.push({ url, auth: options.headers?.Authorization });
+    if (url.endsWith("/auth/link")) {
+      return loggedInViaCookie ? jsonResponse({ conversations_moved: 1 }) : jsonResponse({}, false, 401);
+    }
+    return jsonResponse({ conversation_id: "c1" });
+  };
+  const tokens = new TokenSource("https://api.example");
+  const client = new AgentChatClient("https://api.example", tokens);
+
+  // Before login: claimVisitorHistory gets 401, pass is kept, bearer old-cookie-pass sent
+  await client.createConversation();
+  const sentWhileSignedOut = calls.filter((c) => c.url.endsWith("/conversations")).pop().auth;
+  assert.equal(sentWhileSignedOut, "Bearer old-cookie-pass", "visitor pass used while signed out");
+
+  // User logs in via cookie on the host site (zero-code: no refreshIdentity/reset called)
+  loggedInViaCookie = true;
+  await client.createConversation();
+  const sentAfterCookieLogin = calls.filter((c) => c.url.endsWith("/conversations")).pop().auth;
+  assert.equal(sentAfterCookieLogin, undefined, "no bearer sent after cookie login");
+  assert.ok(
+    calls.some((c) => c.url.endsWith("/auth/link")),
+    "cookie mode pre-login conversations are merged",
+  );
+  assert.equal(
+    localStorage.getItem(visitorPassKey("https://api.example")),
+    null,
+    "visitor pass is cleared after successful cookie merge",
+  );
+}
+
 // reset() keeps the visitor pass; only forget() discards it. Getting this
 // backwards silently throws away the conversations the merge exists to rescue.
 {
diff --git a/src/agent_manager/api/static/widget/auth/tokenSource.ts b/src/agent_manager/api/static/widget/auth/tokenSource.ts
index 573fab22..642d0ad6 100644
--- a/src/agent_manager/api/static/widget/auth/tokenSource.ts
+++ b/src/agent_manager/api/static/widget/auth/tokenSource.ts
@@ -46,6 +46,8 @@ export class TokenSource {
   /** Bumped by `reset()` so a resolution already in flight, once it lands, can
    *  tell it is answering a question nobody is asking anymore. */
   private generation = 0;
+  /** Avoid repeating unauthenticated claim attempts for the same pass in cookie mode. */
+  private lastClaimAttemptPass: string | null = null;
   private readonly tokenUrl: string;
   private readonly provider: TokenProvider | null;
   private readonly storage: Storage;
@@ -64,7 +66,9 @@ export class TokenSource {
   }
 
   async current(): Promise<string | null> {
-    if (!this.cached) await this.resolve(() => this.storedPass());
+    if (!this.cached || (this.isCookieMode() && this.storedPass() !== null)) {
+      await this.resolve(() => this.storedPass());
+    }
     return this.cached;
   }
 
@@ -114,26 +118,40 @@ export class TokenSource {
     return this.pending;
   }
 
+  private isCookieMode(): boolean {
+    return !this.tokenUrl && !this.provider;
+  }
+
   /** A host token, plus the one-time hand-off of whatever this browser chatted
    *  about before signing in. */
   private async hostToken(): Promise<string | null> {
     const token = await this.fromHost();
-    if (token) await this.claimVisitorHistory(token);
+    if (token || (this.isCookieMode() && this.storedPass())) {
+      await this.claimVisitorHistory(token);
+    }
     return token;
   }
 
-  private async claimVisitorHistory(hostToken: string): Promise<void> {
+  private async claimVisitorHistory(hostToken: string | null): Promise<void> {
     const pass = this.storedPass();
     if (!pass) return;
     try {
+      const headers: Record<string, string> = { "Content-Type": "application/json" };
+      if (hostToken) headers.Authorization = `Bearer ${hostToken}`;
       const response = await fetch(`${this.endpoint}${LINK_ENDPOINT}`, {
         method: "POST",
-        headers: { "Content-Type": "application/json", Authorization: `Bearer ${hostToken}` },
+        headers,
+        credentials: "include",
         body: JSON.stringify({ anonymous_token: pass }),
       });
-      // Drop the pass on any verdict, including a refusal — only a server that
-      // never answered is worth asking again.
-      if (response.status < 500) this.clearPass();
+      if (response.ok) {
+        const data = (await response.json().catch(() => null)) as { conversations_moved?: number } | null;
+        if (hostToken !== null || (data?.conversations_moved ?? 0) > 0) {
+          this.clearPass();
+        }
+      } else if (hostToken !== null && response.status >= 400 && response.status < 500 && response.status !== 401) {
+        this.clearPass();
+      }
     } catch {
       // Offline: keep the pass so the next page load retries the hand-off.
     }
diff --git a/tests/agent_manager/test_api.py b/tests/agent_manager/test_api.py
index 89ff9bee..408abb58 100644
--- a/tests/agent_manager/test_api.py
+++ b/tests/agent_manager/test_api.py
@@ -393,6 +393,49 @@ def test_signing_in_adopts_the_conversations_a_visitor_already_started() -> None
     assert client.get(f"/conversations/{cid}/messages", headers=visitor).status_code == 403
 
 
+def test_linking_via_cookie_authentication() -> None:
+    """In host_token (cookie) mode, /auth/link is called with session cookies."""
+    app = build_test_app(
+        ConversationService(RecordingEngine(), MemoryRepository()),
+        extra_auth_mode=AuthMode.HOST_TOKEN,
+        extra_auth_cookie=HOST_COOKIE,
+        extra_auth_claim_user_id="id",
+    )
+    anon_client = TestClient(app)
+    pass_token = anon_client.post("/auth/anonymous").json()["token"]
+    visitor = {"Authorization": f"Bearer {pass_token}"}
+    cid = anon_client.post("/conversations", headers=visitor).json()["conversation_id"]
+    anon_client.post(
+        f"/conversations/{cid}/messages", json={"message": "hi from visitor"}, headers=visitor
+    )
+
+    alice_client = TestClient(app, cookies=session_cookie(id="alice"))
+    linked = alice_client.post("/auth/link", json={"anonymous_token": pass_token})
+
+    assert linked.status_code == 200
+    assert linked.json() == {"conversations_moved": 1}
+    assert [t["conversation_id"] for t in alice_client.get("/conversations").json()["items"]] == [
+        cid
+    ]
+    assert alice_client.get(f"/conversations/{cid}/messages").status_code == 200
+
+
+def test_linking_via_cookie_returns_401_when_not_logged_in() -> None:
+    """Without a session cookie the server must reject the link request, not silently succeed."""
+    app = build_test_app(
+        ConversationService(RecordingEngine(), MemoryRepository()),
+        extra_auth_mode=AuthMode.HOST_TOKEN,
+        extra_auth_cookie=HOST_COOKIE,
+        extra_auth_claim_user_id="id",
+    )
+    client = TestClient(app)
+    pass_token = client.post("/auth/anonymous").json()["token"]
+
+    # No cookie, no bearer — the server has no way to identify the adopting caller.
+    result = client.post("/auth/link", json={"anonymous_token": pass_token})
+    assert result.status_code == 401
+
+
 def test_linking_refuses_a_pass_that_is_not_ours_or_already_spent() -> None:
     app = build_test_app(ConversationService(RecordingEngine(), MemoryRepository()))
     client = TestClient(app)
diff --git a/tests/e2e/widget.spec.ts b/tests/e2e/widget.spec.ts
index 55e2cf37..9c9eee4c 100644
--- a/tests/e2e/widget.spec.ts
+++ b/tests/e2e/widget.spec.ts
@@ -26,6 +26,14 @@ async function mockConversationApi(
   const calls: string[] = [];
   await pinVisitorPass(page);
 
+  await page.route("**/auth/link", async (route) => {
+    await route.fulfill({
+      status: 200,
+      contentType: "application/json",
+      body: JSON.stringify({ conversations_moved: 0 }),
+    });
+  });
+
   await page.route(/\/conversations\?/, async (route) => {
     calls.push(`GET ${new URL(route.request().url()).pathname}`);
     await route.fulfill({
@@ -1461,3 +1469,40 @@ test("thread drawer paginates and appends next pages on scroll", async ({ page }
 
   await expect.poll(() => shadowText(page, ".thread-drawer")).toContain("Thread Three");
 });
+
+test("visitor pass cached, cookie login hand-off merges history and first thread list request observes merged threads", async ({ page }) => {
+  const calls: string[] = [];
+  await pinVisitorPass(page);
+
+  let linkCalled = false;
+  await page.route("**/auth/link", async (route) => {
+    linkCalled = true;
+    calls.push(`POST ${new URL(route.request().url()).pathname}`);
+    await route.fulfill({
+      status: 200,
+      contentType: "application/json",
+      body: JSON.stringify({ conversations_moved: 1 }),
+    });
+  });
+
+  await page.route(/\/conversations\?/, async (route) => {
+    calls.push(`GET ${new URL(route.request().url()).pathname}`);
+    await route.fulfill({
+      status: 200,
+      contentType: "application/json",
+      body: JSON.stringify({
+        items: linkCalled
+          ? [{ conversation_id: "merged-thread", title: "Merged Thread", last_message_at: "2026-06-28T00:00:00Z" }]
+          : [],
+        next_cursor: null,
+      }),
+    });
+  });
+
+  await page.goto("/widget-demo.html");
+  await shadowClick(page, ".launcher");
+  await shadowClick(page, '[aria-label="Conversations"]');
+
+  await expect.poll(() => linkCalled).toBe(true);
+  await expect.poll(() => shadowText(page, ".thread-drawer")).toContain("Merged Thread");
+});