diff --git a/changes/2157.fix.md b/changes/2157.fix.md
new file mode 100644
index 00000000000..c3fb0e63f71
--- /dev/null
+++ b/changes/2157.fix.md
@@ -0,0 +1 @@
+Correctly register and deregister Agent's terminating kernels
diff --git a/src/ai/backend/agent/agent.py b/src/ai/backend/agent/agent.py
index ea489995482..06989a2a8e7 100644
--- a/src/ai/backend/agent/agent.py
+++ b/src/ai/backend/agent/agent.py
@@ -997,7 +997,6 @@ async def _handle_destroy_event(self, ev: ContainerLifecycleEvent) -> None:
             assert current_task is not None
             if ev.kernel_id not in self._ongoing_destruction_tasks:
                 self._ongoing_destruction_tasks[ev.kernel_id] = current_task
-            self.terminating_kernels.add(ev.kernel_id)
             async with self.registry_lock:
                 kernel_obj = self.kernel_registry.get(ev.kernel_id)
                 if kernel_obj is None:
@@ -1023,6 +1022,7 @@ async def _handle_destroy_event(self, ev: ContainerLifecycleEvent) -> None:
                     if kernel_obj.runner is not None:
                         await kernel_obj.runner.close()
                     kernel_obj.clean_event = ev.done_future
+                self.terminating_kernels.add(ev.kernel_id)
                 try:
                     await self.destroy_kernel(ev.kernel_id, ev.container_id)
                 except Exception as e:
@@ -1042,6 +1042,10 @@ async def _handle_destroy_event(self, ev: ContainerLifecycleEvent) -> None:
                                 done_future=ev.done_future,
                             ),
                         )
+                    else:
+                        # Items in `terminating_kernels` are deleted only in _handle_clean_event()
+                        # Should delete the kernel_id that will not be cleaned
+                        self.terminating_kernels.discard(ev.kernel_id)
         except asyncio.CancelledError:
             pass
         except Exception:
@@ -1304,7 +1308,7 @@ async def sync_container_lifecycles(self, interval: float) -> None:
                         LifecycleEvent.CLEAN,
                         KernelLifecycleEventReason.SELF_TERMINATED,
                     )
-                # Check if: there are containers not spawned by me.
+                # Check if: there are containers not spawned by me or already deleted from my registry.
                 for kernel_id in alive_kernels.keys() - known_kernels.keys():
                     if kernel_id in self.restarting_kernels:
                         continue