diff --git a/tests/test_tui_gateway_server.py b/tests/test_tui_gateway_server.py
index 136703e1042..7998af7292c 100644
--- a/tests/test_tui_gateway_server.py
+++ b/tests/test_tui_gateway_server.py
@@ -107,6 +107,64 @@ def test_session_context_explicit_cwd_for_ephemeral_task(monkeypatch, tmp_path):
         server._clear_session_context(tokens)
 
 
+def _write_profile_cfg(home: Path, cwd: str | None) -> Path:
+    import yaml
+
+    home.mkdir(parents=True, exist_ok=True)
+    cfg = {"terminal": {"cwd": cwd}} if cwd is not None else {}
+    (home / "config.yaml").write_text(yaml.safe_dump(cfg), encoding="utf-8")
+    return home
+
+
+def test_profile_configured_cwd_reads_target_profile(tmp_path):
+    """A profile's own terminal.cwd is read from its config.yaml."""
+    project = tmp_path / "proj"
+    project.mkdir()
+    home = _write_profile_cfg(tmp_path / "home", str(project))
+    assert server._profile_configured_cwd(home) == str(project)
+
+
+def test_profile_configured_cwd_skips_placeholders_and_missing(tmp_path):
+    """Placeholder values, missing config, and bad paths fall through to None."""
+    assert server._profile_configured_cwd(None) is None
+    assert server._profile_configured_cwd(tmp_path / "nope") is None
+    for placeholder in (".", "auto", "cwd", ""):
+        home = _write_profile_cfg(tmp_path / placeholder.strip("."), placeholder)
+        assert server._profile_configured_cwd(home) is None
+    home = _write_profile_cfg(tmp_path / "ghost", str(tmp_path / "does-not-exist"))
+    assert server._profile_configured_cwd(home) is None
+
+
+def test_completion_cwd_prefers_profile_over_stale_env(monkeypatch, tmp_path):
+    """Issue #40334: a new session bound to another profile must use THAT
+    profile's terminal.cwd, not the launch profile's stale TERMINAL_CWD."""
+    profile_b = tmp_path / "ef-design"
+    profile_b.mkdir()
+    home = _write_profile_cfg(tmp_path / "home-b", str(profile_b))
+    stale = tmp_path / "mahjong"
+    stale.mkdir()
+
+    monkeypatch.setenv("TERMINAL_CWD", str(stale))
+    monkeypatch.setattr(server, "_profile_home", lambda name: home if name else None)
+
+    assert server._completion_cwd({"profile": "ef-design"}) == str(profile_b)
+    # No profile → unchanged fallback to the launch env var.
+    assert server._completion_cwd({}) == str(stale)
+
+
+def test_completion_cwd_explicit_cwd_wins_over_profile(monkeypatch, tmp_path):
+    """An explicit client-provided cwd still beats the profile config."""
+    explicit = tmp_path / "explicit"
+    explicit.mkdir()
+    profile_b = tmp_path / "configured"
+    profile_b.mkdir()
+    home = _write_profile_cfg(tmp_path / "home-c", str(profile_b))
+
+    monkeypatch.setattr(server, "_profile_home", lambda name: home if name else None)
+    result = server._completion_cwd({"cwd": str(explicit), "profile": "ef-design"})
+    assert result == str(explicit)
+
+
 def test_terminal_task_cwd_local_backend_uses_session_cwd(monkeypatch, tmp_path):
     """A local terminal backend must keep host-validated session cwd behaviour."""
     project = tmp_path / "project"
diff --git a/tui_gateway/server.py b/tui_gateway/server.py
index 5df9e51de29..69c662d6409 100644
--- a/tui_gateway/server.py
+++ b/tui_gateway/server.py
@@ -688,6 +688,40 @@ def _profile_home(profile: str | None) -> Path | None:
     return home if (home / "state.db").exists() or home.exists() else None
 
 
+# Placeholder ``terminal.cwd`` values that don't name a real directory — the
+# gateway resolves these to the home dir at runtime, so they must NOT be treated
+# as an explicit workspace (mirrors gateway/run.py's config bridge).
+_CWD_PLACEHOLDERS = {".", "auto", "cwd"}
+
+
+def _profile_configured_cwd(profile_home: Path | None) -> str | None:
+    """Resolve a non-launch profile's ``terminal.cwd`` from its own config.yaml.
+
+    The desktop's app-global remote mode serves every profile from one backend,
+    so the process-global ``TERMINAL_CWD`` belongs to the *launch* profile. A new
+    session bound to another profile must take its workspace from THAT profile's
+    config, not the stale env var (issue #40334). Returns an absolute, existing
+    directory, or None for placeholders / missing / invalid paths.
+    """
+    if profile_home is None:
+        return None
+    try:
+        import yaml
+
+        p = Path(profile_home) / "config.yaml"
+        if not p.exists():
+            return None
+        with open(p, encoding="utf-8") as f:
+            data = yaml.safe_load(f) or {}
+        raw = str((data.get("terminal") or {}).get("cwd") or "").strip()
+        if not raw or raw in _CWD_PLACEHOLDERS:
+            return None
+        resolved = os.path.abspath(os.path.expanduser(raw))
+        return resolved if os.path.isdir(resolved) else None
+    except Exception:
+        return None
+
+
 def write_json(obj: dict) -> bool:
     """Emit one JSON frame. Routes via the most-specific transport available.
 
@@ -995,9 +1029,13 @@ def _normalize_completion_path(path_part: str) -> str:
 
 
 def _completion_cwd(params: dict | None = None) -> str:
+    params = params or {}
     raw = (
-        (params or {}).get("cwd")
-        or _sessions.get((params or {}).get("session_id") or "", {}).get("cwd")
+        params.get("cwd")
+        or _sessions.get(params.get("session_id") or "", {}).get("cwd")
+        # A session bound to another profile resolves its workspace from THAT
+        # profile's config before falling back to the launch profile's env var.
+        or _profile_configured_cwd(_profile_home(params.get("profile")))
         or os.environ.get("TERMINAL_CWD")
         or os.getcwd()
     )