diff --git a/hermes_cli/active_sessions.py b/hermes_cli/active_sessions.py
index 7fdb9c2d729..7eba80e5024 100644
--- a/hermes_cli/active_sessions.py
+++ b/hermes_cli/active_sessions.py
@@ -78,7 +78,7 @@ def active_session_limit_message(active_count: int, max_sessions: int) -> str:
 
 
 def _state_dir() -> Path:
-    return get_hermes_home() / "runtime"
+    return Path(get_hermes_home()) / "runtime"
 
 
 def _state_path() -> Path:
@@ -311,6 +311,43 @@ def release_active_session(lease: ActiveSessionLease) -> None:
         lease.released = True
 
 
+def transfer_active_session(
+    lease: ActiveSessionLease,
+    *,
+    session_id: str,
+    metadata: Optional[dict[str, Any]] = None,
+) -> bool:
+    """Move an existing lease to a new session id without dropping the slot."""
+    new_session_id = str(session_id or "")
+    if not new_session_id:
+        return False
+    if lease.released:
+        return False
+    if not lease.enabled:
+        lease.session_id = new_session_id
+        return True
+
+    state_path = _state_path()
+    with _FileLock(_lock_path()):
+        entries = _prune_dead(_read_entries(state_path))
+        updated = False
+        for entry in entries:
+            if str(entry.get("lease_id") or "") != lease.lease_id:
+                continue
+            entry["session_id"] = new_session_id
+            entry["updated_at"] = time.time()
+            if metadata:
+                entry["metadata"] = {
+                    str(k): v for k, v in metadata.items() if isinstance(k, str)
+                }
+            updated = True
+            break
+        if updated:
+            _write_entries(state_path, entries)
+            lease.session_id = new_session_id
+        return updated
+
+
 def active_session_registry_snapshot() -> list[dict[str, Any]]:
     """Return the pruned active-session registry for diagnostics/tests."""
     state_path = _state_path()
diff --git a/tests/hermes_cli/test_active_sessions.py b/tests/hermes_cli/test_active_sessions.py
index 7988f3a0b02..dda461d686b 100644
--- a/tests/hermes_cli/test_active_sessions.py
+++ b/tests/hermes_cli/test_active_sessions.py
@@ -113,6 +113,33 @@ def test_active_session_registry_prunes_dead_pids(tmp_path, monkeypatch):
     lease.release()
 
 
+def test_transfer_active_session_reanchors_existing_lease(tmp_path, monkeypatch):
+    home = tmp_path / ".hermes"
+    monkeypatch.setenv("HERMES_HOME", str(home))
+
+    lease, message = active_sessions.try_acquire_active_session(
+        session_id="session-old",
+        surface="tui",
+        config={"max_concurrent_sessions": 1},
+        metadata={"live_session_id": "ui-1"},
+    )
+
+    assert message is None
+    assert lease is not None
+    assert active_sessions.transfer_active_session(
+        lease,
+        session_id="session-new",
+        metadata={"live_session_id": "ui-1"},
+    )
+
+    snapshot = active_sessions.active_session_registry_snapshot()
+    assert lease.session_id == "session-new"
+    assert len(snapshot) == 1
+    assert snapshot[0]["session_id"] == "session-new"
+    assert snapshot[0]["metadata"] == {"live_session_id": "ui-1"}
+    lease.release()
+
+
 def test_pid_alive_uses_safe_pid_exists_without_signalling(monkeypatch):
     checked: list[int] = []
 
diff --git a/tests/tui_gateway/test_protocol.py b/tests/tui_gateway/test_protocol.py
index 775a07cb317..054fc4df09f 100644
--- a/tests/tui_gateway/test_protocol.py
+++ b/tests/tui_gateway/test_protocol.py
@@ -734,6 +734,100 @@ def test_session_resume_reuses_existing_live_session(server, monkeypatch):
     assert all(sid == winner for sid in server._sessions)
 
 
+def test_session_resume_reuses_live_agent_after_compression_rotation(server, monkeypatch):
+    """Resume must match the live agent's current session_id, not stale session_key."""
+
+    target = "20260409_020202_child"
+    stale_parent = "20260409_010101_parent"
+    sid = "live-rotated"
+    server._sessions[sid] = {
+        "agent": types.SimpleNamespace(model="test/model", session_id=target),
+        "created_at": 123.0,
+        "display_history_prefix": [],
+        "history": [{"role": "assistant", "content": "live child"}],
+        "history_lock": threading.RLock(),
+        "last_active": 123.0,
+        "running": False,
+        "session_key": stale_parent,
+        "transport": server._stdio_transport,
+    }
+
+    class _DB:
+        def get_session(self, _sid):
+            return {"id": target}
+
+        def get_session_by_title(self, _title):
+            return None
+
+        def resolve_resume_session_id(self, _target):
+            return target
+
+    monkeypatch.setattr(server, "_get_db", lambda: _DB())
+    monkeypatch.setattr(server, "_emit", lambda *_args, **_kwargs: None)
+    monkeypatch.setattr(
+        server,
+        "_session_info",
+        lambda _agent, _session=None: {"model": "test/model"},
+    )
+
+    result = server.handle_request(
+        {
+            "id": "r1",
+            "method": "session.resume",
+            "params": {"session_id": target, "cols": 100},
+        }
+    )
+
+    assert "error" not in result
+    assert result["result"]["session_id"] == sid
+    assert result["result"]["session_key"] == target
+    assert len(server._sessions) == 1
+
+
+def test_sync_session_key_after_compress_reanchors_active_session_lease(
+    server, monkeypatch, tmp_path
+):
+    home = tmp_path / ".hermes"
+    monkeypatch.setenv("HERMES_HOME", str(home))
+
+    from hermes_cli.active_sessions import (
+        active_session_registry_snapshot,
+        try_acquire_active_session,
+    )
+
+    lease, message = try_acquire_active_session(
+        session_id="session-old",
+        surface="tui",
+        config={"max_concurrent_sessions": 1},
+        metadata={"live_session_id": "ui-1"},
+    )
+    assert message is None
+    assert lease is not None
+
+    session = {
+        "active_session_lease": lease,
+        "agent": types.SimpleNamespace(session_id="session-new"),
+        "session_key": "session-old",
+    }
+    fake_approval = types.SimpleNamespace(
+        disable_session_yolo=lambda *_args, **_kwargs: None,
+        enable_session_yolo=lambda *_args, **_kwargs: None,
+        is_session_yolo_enabled=lambda *_args, **_kwargs: False,
+        register_gateway_notify=lambda *_args, **_kwargs: None,
+        unregister_gateway_notify=lambda *_args, **_kwargs: None,
+    )
+    monkeypatch.setattr(server, "_restart_slash_worker", lambda *_args, **_kwargs: None)
+
+    with patch.dict(sys.modules, {"tools.approval": fake_approval}):
+        server._sync_session_key_after_compress("ui-1", session)
+
+    snapshot = active_session_registry_snapshot()
+    assert session["session_key"] == "session-new"
+    assert lease.session_id == "session-new"
+    assert [entry["session_id"] for entry in snapshot] == ["session-new"]
+    lease.release()
+
+
 def test_session_resume_live_payload_uses_current_history_with_ancestors(server, monkeypatch):
     """Live resume should not reuse a stale ancestor-inclusive snapshot."""
 
diff --git a/tui_gateway/server.py b/tui_gateway/server.py
index e4bcf1b0bfc..a7e1ba18b75 100644
--- a/tui_gateway/server.py
+++ b/tui_gateway/server.py
@@ -381,6 +381,59 @@ def _release_active_session_slot(session: dict | None) -> None:
         logger.debug("Failed to release active session slot", exc_info=True)
 
 
+def _transfer_active_session_slot(
+    sid: str,
+    session: dict,
+    *,
+    new_session_id: str,
+) -> bool:
+    if not new_session_id:
+        return False
+    lease = session.get("active_session_lease")
+    if lease is None:
+        return True
+    try:
+        from hermes_cli.active_sessions import transfer_active_session
+
+        if transfer_active_session(
+            lease,
+            session_id=new_session_id,
+            metadata={"live_session_id": sid},
+        ):
+            return True
+    except Exception:
+        logger.debug("Failed to transfer active session slot", exc_info=True)
+
+    # Fallback: the in-place transfer could not move the lease (entry pruned /
+    # pid-check transiently failed). Reserve the new slot BEFORE releasing the
+    # old one, so a concurrent gateway at the session cap cannot grab the freed
+    # slot in a release-then-reacquire window and leave this session with no
+    # lease at all (#49041 review). If the reserve fails, KEEP the old lease.
+    new_lease, limit_message = _claim_active_session_slot(
+        new_session_id,
+        live_session_id=sid,
+    )
+    if new_lease is not None:
+        old_lease = session.pop("active_session_lease", None)
+        if old_lease is not None:
+            try:
+                old_lease.release()
+            except Exception:
+                logger.debug("Failed to release stale active session slot", exc_info=True)
+        session["active_session_lease"] = new_lease
+        return True
+    # Reserve failed — retain the existing lease rather than dropping it.
+    if limit_message:
+        logger.warning(
+            "Compression session lease re-anchor failed (kept old lease): "
+            "sid=%s new_session_id=%s reason=%s",
+            sid,
+            new_session_id,
+            limit_message,
+        )
+    return False
+
+
 def _finalize_session(session: dict | None, end_reason: str = "tui_close") -> None:
     """Best-effort finalize hook + memory commit for a session.
 
@@ -2543,6 +2596,19 @@ def _sync_session_key_after_compress(
     if not new_session_id or new_session_id == old_key:
         return
 
+    lease_reanchored = _transfer_active_session_slot(
+        sid,
+        session,
+        new_session_id=new_session_id,
+    )
+    if not lease_reanchored:
+        logger.warning(
+            "Compression session lease did not re-anchor: sid=%s old_session_id=%s new_session_id=%s",
+            sid,
+            old_key,
+            new_session_id,
+        )
+
     try:
         from tools.approval import (
             disable_session_yolo,
@@ -4940,7 +5006,7 @@ def _session_live_title(session: dict, key: str) -> str:
 
 
 def _session_live_item(sid: str, session: dict, current_sid: str = "") -> dict:
-    key = str(session.get("session_key") or sid)
+    key = _session_lookup_key(session, fallback=sid)
     agent = session.get("agent")
     history = list(session.get("history") or [])
     status = _session_live_status(sid, session)
@@ -4964,11 +5030,21 @@ def _session_live_item(sid: str, session: dict, current_sid: str = "") -> dict:
     }
 
 
+def _session_lookup_key(session: dict, *, fallback: str = "") -> str:
+    agent = session.get("agent")
+    return str(
+        getattr(agent, "session_id", None)
+        or session.get("session_key")
+        or fallback
+        or ""
+    )
+
+
 def _find_live_session_by_key(session_key: str) -> tuple[str, dict] | None:
     for sid, session in list(_sessions.items()):
         if session.get("_finalized"):
             continue
-        if str(session.get("session_key") or "") == session_key:
+        if _session_lookup_key(session, fallback=sid) == session_key:
             return sid, session
     return None
 
@@ -5012,7 +5088,7 @@ def _live_session_payload(
         "messages": _history_to_messages(history),
         "running": running,
         "session_id": sid,
-        "session_key": session.get("session_key") or sid,
+        "session_key": _session_lookup_key(session, fallback=sid),
         "started_at": float(session.get("created_at") or time.time()),
         "status": _session_live_status(sid, session),
     }