diff --git a/api/configs/feature/__init__.py b/api/configs/feature/__init__.py
index 12971b9b8ca..5897698d1c8 100644
--- a/api/configs/feature/__init__.py
+++ b/api/configs/feature/__init__.py
@@ -11,6 +11,7 @@ from pydantic import (
     PositiveFloat,
     PositiveInt,
     computed_field,
+    field_validator,
 )
 from pydantic_settings import BaseSettings
 
@@ -280,6 +281,27 @@ class PluginConfig(BaseSettings):
         default="",
     )
 
+    @field_validator("PLUGIN_REMOTE_INSTALL_PORT", mode="before")
+    @classmethod
+    def _reject_host_port_shaped_plugin_remote_install_port(cls, v):
+        """Reject ``host:port``-shaped values with an actionable hint.
+
+        ``EXPOSE_PLUGIN_DEBUGGING_PORT`` is overloaded: it feeds both the
+        plugin_daemon ``ports:`` mapping (where ``127.0.0.1:5003`` is valid
+        compose syntax) and this integer app setting advertised in the console.
+        Without this guard a loopback bind spec crashloops the api container
+        with an opaque ``int_parsing`` traceback. See issue #39323.
+        """
+        if isinstance(v, str) and ":" in v.strip():
+            raise ValueError(
+                "PLUGIN_REMOTE_INSTALL_PORT must be a bare port number, got "
+                f"{v!r}. A 'host:port' value usually means "
+                "EXPOSE_PLUGIN_DEBUGGING_PORT was set to a compose publish spec "
+                "like '127.0.0.1:5003'; bind loopback via a "
+                "docker-compose.override.yaml instead of overloading this var."
+            )
+        return v
+
     @property
     def NEW_USER_DEFAULT_PLUGIN_ID_LIST(self) -> list[str]:
         return [item.strip() for item in self.NEW_USER_DEFAULT_PLUGIN_IDS.split(",") if item.strip()]
diff --git a/api/tests/unit_tests/configs/test_dify_config.py b/api/tests/unit_tests/configs/test_dify_config.py
index 49934cf4837..3588f6beef1 100644
--- a/api/tests/unit_tests/configs/test_dify_config.py
+++ b/api/tests/unit_tests/configs/test_dify_config.py
@@ -109,6 +109,24 @@ def test_new_user_default_plugin_ids_are_parsed_from_env(monkeypatch: pytest.Mon
     ]
 
 
+def test_plugin_remote_install_port_rejects_host_port_spec(monkeypatch: pytest.MonkeyPatch) -> None:
+    """A 'host:port' compose publish spec must produce an actionable error, not an opaque int_parsing traceback."""
+    _set_basic_config_env(monkeypatch)
+    monkeypatch.setenv("PLUGIN_REMOTE_INSTALL_PORT", "127.0.0.1:5003")
+
+    with pytest.raises(ValueError, match="must be a bare port number"):
+        DifyConfig(_env_file=None)
+
+
+def test_plugin_remote_install_port_accepts_bare_port(monkeypatch: pytest.MonkeyPatch) -> None:
+    _set_basic_config_env(monkeypatch)
+    monkeypatch.setenv("PLUGIN_REMOTE_INSTALL_PORT", "5003")
+
+    config = DifyConfig(_env_file=None)
+
+    assert config.PLUGIN_REMOTE_INSTALL_PORT == 5003
+
+
 def test_new_user_default_models_are_parsed_from_env(monkeypatch: pytest.MonkeyPatch) -> None:
     _set_basic_config_env(monkeypatch)
     monkeypatch.setenv(