diff --git a/agent-chat/server.ts b/agent-chat/server.ts
index 12711e98d55a..7e42381ddeac 100644
--- a/agent-chat/server.ts
+++ b/agent-chat/server.ts
@@ -16,7 +16,7 @@ import { claudeAdapter } from "./adapters/claude";
 import { codexAdapter } from "./adapters/codex";
 import { piAdapter } from "./adapters/pi";
 import { makeAcpAdapter } from "./adapters/acp";
-import { attachTranscript, focusTranscriptTerminal, transcriptAdapter, type TranscriptAgent } from "./adapters/transcript";
+import { attachTranscript, focusTranscriptTerminal, transcriptAdapter, transcriptTarget, type TranscriptAgent } from "./adapters/transcript";
 import { resolveSessionTranscript, resolveSurfaceTranscript, transcriptAttention, type TranscriptSource } from "./transcript-sources";
 import { pickAccentColor, resolveGhosttyTheme, resolveGhosttyThemeAsync, type GhosttyTheme } from "./theme";
 import { agentModelCatalog, type AgentModelProviderCatalog } from "./catalog";
@@ -644,7 +644,15 @@ function transcriptTitle(source: TranscriptSource): string {
 function ensureTranscriptSession(source: TranscriptSource): Session {
   const id = transcriptSessionId(source);
   const existing = sessions.get(id);
-  if (existing?.transcript?.path === source.path) return existing;
+  if (existing?.transcript?.path === source.path) {
+    const target = transcriptTarget(existing);
+    if (target?.agentSessionId !== source.sessionId || target?.surfaceId !== source.surfaceId) {
+      // A resumed agent can keep its transcript while moving to another
+      // terminal. Replace changed bindings to also fence old RPC replies.
+      existing.internal.transcriptTarget = { agentSessionId: source.sessionId, surfaceId: source.surfaceId };
+    }
+    return existing;
+  }
   if (existing?.transcript) {
     // The agent's transcript moved (for example a resolved fallback path):
     // re-point the same session so open pages stay subscribed.
@@ -667,6 +675,10 @@ function ensureTranscriptSession(source: TranscriptSource): Session {
   return sess;
 }
 
+export function ensureTranscriptSessionForTest(source: TranscriptSource): Session {
+  return ensureTranscriptSession(source);
+}
+
 function startTranscriptTail(sess: Session, source: TranscriptSource) {
   attachTranscript(sess, source.agent, source.path, (title) => {
     if (sess.title === title) return;
@@ -2156,6 +2168,10 @@ function sendWsErrorDetails(
   ws.send(JSON.stringify({ kind: "error", op, message: safeErrorMessage(op, err, { provider }), ...publicDetails }));
 }
 
+export function handleMessageForTest(ws: Bun.ServerWebSocket<WsData>, msg: any) {
+  handleMessage(ws, msg);
+}
+
 function handleMessage(ws: Bun.ServerWebSocket<WsData>, msg: any) {
   switch (msg.op) {
     case "start": {
@@ -2232,7 +2248,10 @@ function handleMessage(ws: Bun.ServerWebSocket<WsData>, msg: any) {
     }
     case "subscribe": {
       const sessionId = String(msg.sessionId);
-      const sess = sessions.get(sessionId) ?? resolveTranscriptSessionById(sessionId);
+      // The agent may have resumed elsewhere while this page was offline.
+      // Refresh terminal transcript bindings even when the session is cached;
+      // retain cached history if the hook record is temporarily unavailable.
+      const sess = resolveTranscriptSessionById(sessionId) ?? sessions.get(sessionId);
       if (!sess) {
         ws.send(JSON.stringify({ kind: "no-session", sessionId: msg.sessionId }));
         return;
diff --git a/agent-chat/test/transcript-reconnect.test.ts b/agent-chat/test/transcript-reconnect.test.ts
new file mode 100644
index 000000000000..2d3a4ed38891
--- /dev/null
+++ b/agent-chat/test/transcript-reconnect.test.ts
@@ -0,0 +1,84 @@
+import assert from "node:assert/strict";
+import { mkdir, mkdtemp, rm, writeFile } from "node:fs/promises";
+import { join } from "node:path";
+import { ensureTranscriptSessionForTest, handleMessageForTest } from "../server";
+import { setTranscriptRpcForTest, transcriptAdapter, type TranscriptTail } from "../adapters/transcript";
+import type { TranscriptSource } from "../transcript-sources";
+import type { SessionCtx } from "../types";
+
+const priorHooks = process.env.CMUX_AGENT_HOOK_STATE_DIR;
+const priorClaude = process.env.CMUX_CLAUDE_HOOK_STATE_PATH;
+const sessions: SessionCtx[] = [];
+let root: string | undefined;
+try {
+  const scratch = join(import.meta.dir, "../scratch");
+  await mkdir(scratch, { recursive: true });
+  root = await mkdtemp(join(scratch, "transcript-reconnect-"));
+  process.env.CMUX_AGENT_HOOK_STATE_DIR = root;
+  delete process.env.CMUX_CLAUDE_HOOK_STATE_PATH;
+  await Promise.all(["claude", "codex"].map((agent) => writeFile(join(root!, `${agent}-hook-sessions.json`), "{}")));
+  for (const agent of ["claude", "codex"] as const) {
+    const oldPath = join(root, `${agent}-old.jsonl`);
+    const newPath = join(root, `${agent}-new.jsonl`);
+    await Promise.all([oldPath, newPath].map((path) => writeFile(path, "")));
+    const source: TranscriptSource = { agent, path: oldPath, sessionId: crypto.randomUUID(), surfaceId: "OLD-SURFACE", updatedAt: 1 };
+    const sess = ensureTranscriptSessionForTest(source);
+    sessions.push(sess);
+    await (sess.internal.transcript as { tail: TranscriptTail }).tail.poll();
+    sess.events.push({ kind: "user", text: "cached history" });
+    const attachment = sess.internal.transcript;
+    const messages: any[] = [];
+    const ws = {
+      data: { subscribed: null as string | null },
+      send(payload: string) { messages.push(JSON.parse(payload)); return 1; },
+    } as unknown as Parameters<typeof handleMessageForTest>[0];
+    const subscribe = () => { messages.length = 0; handleMessageForTest(ws, { op: "subscribe", sessionId: sess.id }); };
+    const store = join(root, `${agent}-hook-sessions.json`);
+    const record = async (path: string) => writeFile(store, JSON.stringify({ sessions: {
+      [source.sessionId]: { surfaceId: "NEW-SURFACE", transcriptPath: path, updatedAt: 2 },
+    } }));
+    await record(oldPath);
+    subscribe();
+    assert.equal(ws.data.subscribed, sess.id);
+    assert.deepEqual(messages.find((message) => message.kind === "history")?.events, [{ kind: "user", text: "cached history" }]);
+    assert.equal(sess.internal.transcript, attachment, "same-path reconnect preserves the existing reader");
+    const calls: Record<string, unknown>[] = [];
+    setTranscriptRpcForTest(async (method, params) => { calls.push({ method, ...params }); return { ok: true }; });
+    handleMessageForTest(ws, { op: "focus-terminal", sessionId: sess.id });
+    await Promise.resolve();
+    assert.equal(calls[0]?.surface_id, "NEW-SURFACE", "reconnecting a cached transcript must refresh its terminal binding");
+
+    // Reconnection must also reattach if the hook now points at another file.
+    await record(newPath);
+    subscribe();
+    await (sess.internal.transcript as { tail: TranscriptTail }).tail.poll();
+    assert.deepEqual(messages.find((message) => message.kind === "history")?.events, [], "the old file's history must not replay after transcript redirection");
+    const line = agent === "claude"
+      ? { type: "user", uuid: "fresh", message: { role: "user", content: "new transcript input" } }
+      : { type: "event_msg", payload: { type: "user_message", message: "new transcript input" } };
+    await writeFile(newPath, JSON.stringify(line) + "\n");
+    await (sess.internal.transcript as { tail: TranscriptTail }).tail.poll();
+    assert.equal(messages.some((message) => message.kind === "event" && message.evt?.text === "new transcript input"), true, "the connected page receives events from the new transcript");
+
+    // A temporarily unavailable hook record must not discard usable history.
+    await writeFile(store, "{}");
+    subscribe();
+    assert.equal(messages.some((message) => message.kind === "no-session"), false);
+    assert.equal(messages.find((message) => message.kind === "history")?.events.some((event: any) => event.text === "new transcript input"), true);
+    handleMessageForTest(ws, { op: "delete", sessionId: sess.id });
+    transcriptAdapter.dispose(sess);
+  }
+  const missingMessages: any[] = [];
+  const missingWs = { data: { subscribed: null }, send(payload: string) { missingMessages.push(JSON.parse(payload)); return 1; } } as unknown as Parameters<typeof handleMessageForTest>[0];
+  handleMessageForTest(missingWs, { op: "subscribe", sessionId: "t-missing-session-id" });
+  assert.deepEqual(missingMessages, [{ kind: "no-session", sessionId: "t-missing-session-id" }]);
+  console.log("Claude and Codex reconnects refresh cached bindings and transcript paths, stream new history, and retain cached history on hook misses: OK");
+} finally {
+  setTranscriptRpcForTest(null);
+  for (const sess of sessions) transcriptAdapter.dispose(sess);
+  if (priorHooks === undefined) delete process.env.CMUX_AGENT_HOOK_STATE_DIR;
+  else process.env.CMUX_AGENT_HOOK_STATE_DIR = priorHooks;
+  if (priorClaude === undefined) delete process.env.CMUX_CLAUDE_HOOK_STATE_PATH;
+  else process.env.CMUX_CLAUDE_HOOK_STATE_PATH = priorClaude;
+  if (root) await rm(root, { recursive: true, force: true });
+}
diff --git a/agent-chat/test/transcript-terminal-rebind.test.ts b/agent-chat/test/transcript-terminal-rebind.test.ts
new file mode 100644
index 000000000000..e13fd256b483
--- /dev/null
+++ b/agent-chat/test/transcript-terminal-rebind.test.ts
@@ -0,0 +1,63 @@
+import assert from "node:assert/strict";
+import { mkdir, mkdtemp, rm, writeFile } from "node:fs/promises";
+import { join } from "node:path";
+import { ensureTranscriptSessionForTest } from "../server";
+import { focusTranscriptTerminal, setTranscriptRpcForTest, transcriptAdapter } from "../adapters/transcript";
+import type { TranscriptSource } from "../transcript-sources";
+import type { CmuxRpcResult } from "../cmux-rpc";
+import type { SessionCtx } from "../types";
+
+const sessions: SessionCtx[] = [];
+let root: string | undefined;
+try {
+  const scratch = join(import.meta.dir, "../scratch");
+  await mkdir(scratch, { recursive: true });
+  root = await mkdtemp(join(scratch, "terminal-rebind-"));
+  for (const agent of ["claude", "codex"] as const) {
+    const path = join(root, `${agent}.jsonl`);
+    await writeFile(path, "");
+    const source: TranscriptSource = { agent, path, sessionId: crypto.randomUUID(), surfaceId: "old-terminal", updatedAt: 1 };
+    const sess = ensureTranscriptSessionForTest(source);
+    sessions.push(sess);
+    sess.events.push({ kind: "user", text: "existing history" });
+    const attachment = sess.internal.transcript;
+
+    let finishOldFocus!: (result: CmuxRpcResult) => void;
+    setTranscriptRpcForTest(() => new Promise((resolve) => { finishOldFocus = resolve; }));
+    const oldFocus = focusTranscriptTerminal(sess);
+
+    const reopened = ensureTranscriptSessionForTest({ ...source, surfaceId: "new-terminal", updatedAt: 2 });
+    assert.equal(reopened, sess, "reopening preserves the session and its subscribers");
+    assert.equal(sess.internal.transcript, attachment, "rebinding does not restart transcript history");
+    const calls: { method: string; params: Record<string, unknown> }[] = [];
+    setTranscriptRpcForTest(async (method, params) => { calls.push({ method, params }); return { ok: true }; });
+    await focusTranscriptTerminal(reopened);
+    assert.equal(calls.length, 1);
+    assert.equal(calls[0].method, "surface.focus");
+    assert.equal(calls[0].params.surface_id, "new-terminal", "reopening the same transcript must focus its current terminal");
+    finishOldFocus({ ok: false, error: "old terminal disappeared" });
+    await oldFocus;
+    assert.deepEqual(sess.events, [{ kind: "user", text: "existing history" }], "the previous terminal's reply must not contaminate the reopened view");
+
+    // Repeated resolution with identical IDs must not discard a valid reply.
+    setTranscriptRpcForTest(() => new Promise((resolve) => { finishOldFocus = resolve; }));
+    const currentFocus = focusTranscriptTerminal(sess);
+    ensureTranscriptSessionForTest({ ...source, surfaceId: "new-terminal", updatedAt: 3 });
+    finishOldFocus({ ok: false, error: "current terminal failed" });
+    await currentFocus;
+    assert.equal(sess.events.length, 2, "unchanged bindings still report their own failures");
+
+    const detached = ensureTranscriptSessionForTest({ ...source, surfaceId: undefined, updatedAt: 4 });
+    calls.length = 0;
+    setTranscriptRpcForTest(async (method, params) => { calls.push({ method, params }); return { ok: true }; });
+    const detachedFocus = await focusTranscriptTerminal(detached);
+    assert.equal(detachedFocus.ok, false, "a removed surface must not retain a focus destination");
+    assert.deepEqual(calls, [], "a removed binding must never focus the stale terminal");
+    transcriptAdapter.dispose(sess);
+  }
+  console.log("Reopening Claude and Codex transcripts refreshes terminal focus without resetting history or accepting stale failures: OK");
+} finally {
+  setTranscriptRpcForTest(null);
+  for (const sess of sessions) transcriptAdapter.dispose(sess);
+  if (root) await rm(root, { recursive: true, force: true });
+}