diff --git a/apps/agent-worker/src/terminal-token.ts b/apps/agent-worker/src/terminal-token.ts
index 98aeace..90ae713 100644
--- a/apps/agent-worker/src/terminal-token.ts
+++ b/apps/agent-worker/src/terminal-token.ts
@@ -28,6 +28,18 @@ export const verifyTerminalToken = (
   );
 };
 
+// Extract the username a box token authorizes without verifying its signature.
+// The token itself authorizes the connection, so the upgrade handler reads the
+// username from it (rather than a query param) and then verifies the whole
+// token against that username. Returns null unless the format matches
+// `${expiresAtMs}.box.${username}.${hmacSha256Hex}`.
+export const parseBoxTokenUsername = (token: string): string | null => {
+  const parts = token.split('.');
+  if (parts.length !== 4 || parts[1] !== 'box') return null;
+  const username = parts[2];
+  return username ? username : null;
+};
+
 // User-scoped variant authorizing a terminal connection to a user's box.
 // Embeds a literal `box` segment so its four parts never collide with the
 // three-part job token above. Format:
diff --git a/apps/agent-worker/src/terminal.ts b/apps/agent-worker/src/terminal.ts
index b9d4c62..b3e9a19 100644
--- a/apps/agent-worker/src/terminal.ts
+++ b/apps/agent-worker/src/terminal.ts
@@ -4,10 +4,16 @@ import type { WebSocket } from 'ws';
 import { WebSocketServer } from 'ws';
 
 import type { BoxHandle } from './user-container';
+import { boxHomePaths } from './box';
 import { env } from './env';
 import { getDockerClient } from './runtime/docker';
-import { verifyTerminalToken } from './terminal-token';
+import {
+  parseBoxTokenUsername,
+  verifyBoxTerminalToken,
+  verifyTerminalToken,
+} from './terminal-token';
 import { acquireUserBox } from './user-container';
+import { ensureBashProfile } from './user-environment';
 import { getTerminalWorkspace } from './worker';
 
 const clampDimension = (value: unknown) => {
@@ -37,16 +43,36 @@ export const parseResizeMessage = (
   }
 };
 
-const bridge = async (ws: WebSocket, jobId: string) => {
-  const workspace = getTerminalWorkspace(jobId);
-  if (!workspace) {
-    ws.close(1011, 'Workspace is not active.');
-    return;
-  }
+// The login-shell command shared by the job and box terminals: prefer a
+// resumable tmux session, else fall back to a plain interactive login shell.
+const SHELL_CMD = [
+  '/bin/bash',
+  '-lc',
+  'if command -v tmux >/dev/null 2>&1; then exec tmux new-session -A -s spoon; else exec bash -il; fi',
+];
 
-  // Register the message handler immediately and buffer input/size until the exec
-  // is ready (acquiring the box can take seconds on first connect), so the initial
-  // resize and early keystrokes aren't dropped.
+type ShellBridgeOptions = {
+  // Acquire the per-user box (reference-counted); its handle is released on
+  // cleanup. Called after the input handler is wired so early keystrokes buffer.
+  acquire: () => Promise<BoxHandle>;
+  // Host-side preparation before the shell starts (e.g. seed .bash_profile).
+  prepare?: () => Promise<void>;
+  // Directory the login shell starts in (container path).
+  cwd: string;
+  // Env entries appended after TERM (e.g. HOME, and job secrets for job terms).
+  envFlags: string[];
+};
+
+/**
+ * Shared PTY bridge: wire a WebSocket to an interactive login shell running via
+ * a real TTY (dockerode `exec` with `Tty:true` + `exec.resize`) inside the
+ * user's box. Registers the input handler immediately and buffers input/size
+ * until the exec is ready (acquiring the box can take seconds on first connect),
+ * so the initial resize and early keystrokes aren't dropped. Used by both the
+ * job terminal (`bridge`) and the box terminal (`bridgeBox`); only the box to
+ * acquire, the working directory, and the env differ.
+ */
+const runShellBridge = async (ws: WebSocket, opts: ShellBridgeOptions) => {
   const execHolder: {
     current?: { exec: import('dockerode').Exec; stream: Duplex };
   } = {};
@@ -87,11 +113,8 @@ const bridge = async (ws: WebSocket, jobId: string) => {
   // the terminal share the exact same container (Phase 2).
   let boxName: string;
   try {
-    const handle = await acquireUserBox({
-      username: workspace.username,
-      workdir: workspace.workdir,
-      containerHome: workspace.containerHome,
-    });
+    if (opts.prepare) await opts.prepare();
+    const handle = await opts.acquire();
     handleHolder.current = handle;
     boxName = handle.boxName;
   } catch (error) {
@@ -115,17 +138,9 @@ const bridge = async (ws: WebSocket, jobId: string) => {
     AttachStdout: true,
     AttachStderr: true,
     Tty: true,
-    Cmd: [
-      '/bin/bash',
-      '-lc',
-      'if command -v tmux >/dev/null 2>&1; then exec tmux new-session -A -s spoon; else exec bash -il; fi',
-    ],
-    Env: [
-      'TERM=xterm-256color',
-      `HOME=${workspace.containerHome}`,
-      ...workspace.secrets.map((secret) => `${secret.name}=${secret.value}`),
-    ],
-    WorkingDir: workspace.containerRepo,
+    Cmd: SHELL_CMD,
+    Env: ['TERM=xterm-256color', ...opts.envFlags],
+    WorkingDir: opts.cwd,
   });
   const stream = await exec.start({ hijack: true, stdin: true, Tty: true });
   execHolder.current = { exec, stream };
@@ -153,10 +168,47 @@ const bridge = async (ws: WebSocket, jobId: string) => {
   });
 };
 
+// Job terminal: opens the shell at the repo checkout, with the job's selected
+// secrets in the environment (it is scoped to that job's active workspace).
+const bridge = async (ws: WebSocket, jobId: string) => {
+  const workspace = getTerminalWorkspace(jobId);
+  if (!workspace) {
+    ws.close(1011, 'Workspace is not active.');
+    return;
+  }
+  await runShellBridge(ws, {
+    acquire: () =>
+      acquireUserBox({
+        username: workspace.username,
+        workdir: workspace.workdir,
+        containerHome: workspace.containerHome,
+      }),
+    cwd: workspace.containerRepo,
+    envFlags: [
+      `HOME=${workspace.containerHome}`,
+      ...workspace.secrets.map((secret) => `${secret.name}=${secret.value}`),
+    ],
+  });
+};
+
+// Box terminal: opens a login shell rooted at the user's home (`~`), with no
+// per-job secrets — it is user-scoped, not tied to any job's workspace.
+const bridgeBox = async (ws: WebSocket, username: string) => {
+  const { homeDir, containerHome } = boxHomePaths(username);
+  await runShellBridge(ws, {
+    prepare: () => ensureBashProfile(homeDir),
+    acquire: () =>
+      acquireUserBox({ username, workdir: homeDir, containerHome }),
+    cwd: containerHome,
+    envFlags: [`HOME=${containerHome}`],
+  });
+};
+
 /**
- * Attaches the interactive-terminal WebSocket endpoint to the worker's HTTP
- * server. Browser connects to `/jobs/:jobId/terminal?token=…` with a short-lived
- * token minted by the Next app (which has already verified job ownership).
+ * Attaches the interactive-terminal WebSocket endpoints to the worker's HTTP
+ * server. Two routes, each authorized by a short-lived token minted by the Next
+ * app: `/jobs/:jobId/terminal?token=…` (job-scoped, after ownership check) and
+ * `/box/terminal?token=…` (user-scoped, username read from the token itself).
  */
 export const attachTerminalServer = (server: Server) => {
   if (env.runtime !== 'docker') return;
@@ -164,13 +216,34 @@ export const attachTerminalServer = (server: Server) => {
 
   server.on('upgrade', (request, socket, head) => {
     const url = new URL(request.url ?? '', `http://localhost:${env.httpPort}`);
+    const token = url.searchParams.get('token') ?? '';
+
+    // User-scoped box terminal: the token authorizes the connection, so the
+    // username is read FROM the token, then verified against the whole token.
+    if (url.pathname === '/box/terminal') {
+      const username = parseBoxTokenUsername(token);
+      if (
+        !username ||
+        !verifyBoxTerminalToken(token, username, env.terminalSecret)
+      ) {
+        socket.write('HTTP/1.1 401 Unauthorized\r\n\r\n');
+        socket.destroy();
+        return;
+      }
+      wss.handleUpgrade(request, socket, head, (ws) => {
+        void bridgeBox(ws, username).catch(() => {
+          if (ws.readyState === ws.OPEN) ws.close();
+        });
+      });
+      return;
+    }
+
     const match = /^\/jobs\/([^/]+)\/terminal$/.exec(url.pathname);
     if (!match?.[1]) {
       socket.destroy();
       return;
     }
     const jobId = decodeURIComponent(match[1]);
-    const token = url.searchParams.get('token') ?? '';
     if (!verifyTerminalToken(token, jobId, env.terminalSecret)) {
       socket.write('HTTP/1.1 401 Unauthorized\r\n\r\n');
       socket.destroy();
diff --git a/apps/agent-worker/src/user-environment.ts b/apps/agent-worker/src/user-environment.ts
index da81712..921fb36 100644
--- a/apps/agent-worker/src/user-environment.ts
+++ b/apps/agent-worker/src/user-environment.ts
@@ -32,6 +32,23 @@ export const fetchUserEnvironment = async (
 
 const shellQuote = (value: string) => `'${value.replaceAll("'", "'\\''")}'`;
 
+/**
+ * A mounted home has no /etc/skel, so login shells wouldn't source ~/.bashrc.
+ * Write a minimal `.bash_profile` (only if absent) so an interactive login
+ * shell — the agent's, or the user's box terminal — loads their environment.
+ * Shared by `materializeUserHome` and the box terminal bridge.
+ */
+export const ensureBashProfile = async (homeDir: string): Promise<void> => {
+  await mkdir(homeDir, { recursive: true });
+  const bashProfile = path.join(homeDir, '.bash_profile');
+  await readFile(bashProfile, 'utf8').catch(async () => {
+    await writeFile(
+      bashProfile,
+      '# Spoon: load ~/.bashrc for login shells.\n[ -f ~/.bashrc ] && . ~/.bashrc\n',
+    );
+  });
+};
+
 /**
  * Materializes the persistent per-user home: a `.bash_profile` so login shells
  * load `~/.bashrc`; (when configured and changed) a clone of the public dotfiles
@@ -47,16 +64,7 @@ export const materializeUserHome = async (args: {
   redact: (value: string) => string;
 }): Promise<void> => {
   const { homeDir, containerHome, boxName, userEnv, redact } = args;
-  await mkdir(homeDir, { recursive: true });
-
-  // A mounted home has no /etc/skel, so ensure login shells source ~/.bashrc.
-  const bashProfile = path.join(homeDir, '.bash_profile');
-  await readFile(bashProfile, 'utf8').catch(async () => {
-    await writeFile(
-      bashProfile,
-      '# Spoon: load ~/.bashrc for login shells.\n[ -f ~/.bashrc ] && . ~/.bashrc\n',
-    );
-  });
+  await ensureBashProfile(homeDir);
 
   if (!userEnv.enabled) return;
 
diff --git a/apps/agent-worker/tests/unit/box-terminal-token.test.ts b/apps/agent-worker/tests/unit/box-terminal-token.test.ts
index 147aeaf..2f1b48c 100644
--- a/apps/agent-worker/tests/unit/box-terminal-token.test.ts
+++ b/apps/agent-worker/tests/unit/box-terminal-token.test.ts
@@ -1,7 +1,10 @@
 import { createHmac } from 'node:crypto';
 import { describe, expect, test } from 'vitest';
 
-import { verifyBoxTerminalToken } from '../../src/terminal-token';
+import {
+  parseBoxTokenUsername,
+  verifyBoxTerminalToken,
+} from '../../src/terminal-token';
 
 const mintBox = (username: string, expiresAt: number, secret: string) => {
   const payload = `${expiresAt}.box.${username}`;
@@ -47,3 +50,27 @@ describe('verifyBoxTerminalToken', () => {
     expect(verifyBoxTerminalToken(jobToken, 'alice', secret)).toBe(false);
   });
 });
+
+describe('parseBoxTokenUsername', () => {
+  test('extracts the username from a well-formed box token', () => {
+    const token = mintBox('alice', Date.now() + 60_000, 'test-secret');
+    expect(parseBoxTokenUsername(token)).toBe('alice');
+  });
+
+  test('returns null for a 3-part job token', () => {
+    expect(parseBoxTokenUsername('123.alice.sig')).toBeNull();
+  });
+
+  test('returns null when the literal box segment is missing', () => {
+    expect(parseBoxTokenUsername('123.notbox.alice.sig')).toBeNull();
+  });
+
+  test('returns null for an empty username segment', () => {
+    expect(parseBoxTokenUsername('123.box..sig')).toBeNull();
+  });
+
+  test('returns null for garbage input', () => {
+    expect(parseBoxTokenUsername('garbage')).toBeNull();
+    expect(parseBoxTokenUsername('')).toBeNull();
+  });
+});