diff --git a/gateway/platforms/api_server.py b/gateway/platforms/api_server.py
index 031b74c33666..ef3554aabf4e 100644
--- a/gateway/platforms/api_server.py
+++ b/gateway/platforms/api_server.py
@@ -40,6 +40,7 @@ Requires:
 """
 
 import asyncio
+import errno
 import hashlib
 import hmac
 import json
@@ -5212,6 +5213,25 @@ class APIServerAdapter(BasePlatformAdapter):
                 await self._runner.cleanup()
                 self._runner = None
                 self._site = None
+                if getattr(exc, "errno", None) == errno.EADDRINUSE:
+                    # A port conflict is a configuration error, not a
+                    # transient blip — another process holds the port for
+                    # its lifetime. A bare ``return False`` makes the
+                    # reconnect watcher in gateway.run treat it as retryable
+                    # and loop forever at the backoff cap (observed: 1568+
+                    # retries over 5 days across multi-profile setups all
+                    # defaulting to the same port, #52132), filling
+                    # errors.log and leaking the adapter's ResponseStore
+                    # fds each retry. Non-retryable drops it from the
+                    # reconnect queue; the operator recovers with
+                    # ``/platform resume api_server`` after changing the port.
+                    self._set_fatal_error(
+                        "api_server_port_in_use",
+                        f"Port {self._port} already in use. Set "
+                        f"platforms.api_server.port in config.yaml to a "
+                        f"different value, then `/platform resume api_server`.",
+                        retryable=False,
+                    )
                 logger.error(
                     "[%s] Could not bind %s:%d: %s. Set a different port in "
                     "config.yaml: platforms.api_server.port",
diff --git a/tests/gateway/test_api_server_bind_guard.py b/tests/gateway/test_api_server_bind_guard.py
index 284f6b289a79..78d039c73d2c 100644
--- a/tests/gateway/test_api_server_bind_guard.py
+++ b/tests/gateway/test_api_server_bind_guard.py
@@ -217,3 +217,29 @@ class TestBindMechanics:
     def test_pre_probe_helper_removed(self):
         """The racy single-family pre-probe must not come back."""
         assert not hasattr(APIServerAdapter, "_port_is_available")
+
+    @pytest.mark.asyncio
+    async def test_port_conflict_sets_non_retryable_fatal_error(self):
+        """A real port conflict (EADDRINUSE) must set a non-retryable fatal
+        error so the reconnect watcher drops the platform from the retry
+        queue instead of looping indefinitely.
+
+        Previously connect() returned bare ``False``, which the reconnect
+        watcher treated as retryable — retrying every 5 minutes forever,
+        filling errors.log and leaking 2 fds per retry (#52132: 1568+
+        retries over 5 days in a multi-profile setup).
+        """
+        port = self._free_port()
+        first = self._make_adapter(port)
+        assert await first.connect() is True
+        second = self._make_adapter(port)
+        try:
+            result = await second.connect()
+            assert result is False
+            assert second.has_fatal_error is True
+            assert second.fatal_error_retryable is False
+            assert second.fatal_error_code == "api_server_port_in_use"
+            assert str(port) in (second.fatal_error_message or "")
+        finally:
+            await first.disconnect()
+            await second.disconnect()