diff --git a/gateway/run_inbound.py b/gateway/run_inbound.py
index bd39387ca0..4a8846ed89 100644
--- a/gateway/run_inbound.py
+++ b/gateway/run_inbound.py
@@ -1309,18 +1309,13 @@ class GatewayInboundMixin:
             # SIGKILL/OOM skips finally, leaving the durable marker for the next unclean startup's
             # recovery pass.
             await self._clear_durable_active_turn(event)
-            # Unconditional, idempotent release without a run_generation guard: evicts the zombie
-            # left when session_reset bumps the generation mid-flight (gen-N's guarded release in
-            # _run_agent returns False; a sentinel-only check would lock forever).
-            self._release_running_agent_state(_quick_key)
+            # Release only this turn's generation. Eviction may immediately admit a replacement
+            # through the cold path; an unconditional release here would then clear the replacement
+            # sentinel/agent and lease. Reset/stop release their stale slot before installing a
+            # successor, preserving reset-zombie cleanup without granting gen-N successor authority.
+            self._release_running_agent_state(_quick_key, run_generation=_run_generation)
             # Turn lease is keyed by (routing key, run generation) so this unwind can only free
             # the lease its own turn acquired, never a newer turn's.
-            # Unconditional release covers every exit path. _release_running_agent_state is idempotent
-            # (pop-on-absent is harmless) and, called without a run_generation guard, always clears the slot
-            # regardless of which generation it holds. This evicts the zombie left when session_reset bumps
-            # the generation (N -> N+1) mid-flight: gen-N's guarded release inside _run_agent returns False,
-            # and the old sentinel-only check here missed the leftover real agent — locking the session out
-            # forever (#28686).
             self._release_turn_lease(_quick_key, _run_generation)
 
     def _restore_moa_one_shot(self, event: "MessageEvent", quick_key: str) -> None:
diff --git a/tests/gateway/test_reaped_eviction_interrupts_run.py b/tests/gateway/test_reaped_eviction_interrupts_run.py
index 1b9b3f1801..42ed2ed61c 100644
--- a/tests/gateway/test_reaped_eviction_interrupts_run.py
+++ b/tests/gateway/test_reaped_eviction_interrupts_run.py
@@ -97,3 +97,22 @@ def test_eviction_cleanup_survives_empty_pending_or_failed_interrupt(agent) -> N
 
     assert state.turn.agent is None
     assert KEY not in gateway._agent_cache
+
+
+def test_stale_finalizer_cannot_release_replacement_generation() -> None:
+    events: list[tuple] = []
+    old_agent = _RecordingAgent(events, lambda: None)
+    gateway, state = _build_gateway(old_agent, events)
+    state.persistent.run_generation = 2
+
+    # Eviction releases generation 2 before the cold path claims the replacement.
+    gateway._invalidate_session_run_generation(KEY, reason="reaped_session_eviction")
+    gateway._release_running_agent_state(KEY)
+    replacement = object()
+    replacement_state = gateway._session_state(KEY)
+    replacement_state.turn.agent = replacement
+    replacement_state.persistent.run_generation = 4
+
+    # Generation 2 is unwinding after generation 4 claimed the key.
+    assert gateway._release_running_agent_state(KEY, run_generation=2) is False
+    assert gateway._peek_session_state(KEY).turn.agent is replacement