diff --git a/gateway/run.py b/gateway/run.py
index 527da4ff5132..9c70fb2d56b9 100644
--- a/gateway/run.py
+++ b/gateway/run.py
@@ -2802,6 +2802,9 @@ class GatewayRunner(GatewayAuthorizationMixin, GatewayKanbanWatchersMixin, Gatew
 
     def __init__(self, config: Optional[GatewayConfig] = None):
         global _gateway_runner_ref
+        # Support dict input for test compatibility; convert to GatewayConfig
+        if config is not None and isinstance(config, dict):
+            config = GatewayConfig(**config)
         self.config = config or load_gateway_config()
         # Mark the process as a profile multiplexer when configured. This flips
         # agent.secret_scope.get_secret() to fail-closed on any unscoped
@@ -13100,6 +13103,33 @@ async def _run_background_task(
         event_message_id: Optional[str] = None,
         media_urls: Optional[List[str]] = None,
         media_types: Optional[List[str]] = None,
+    ) -> None:
+        """Profile-scoping wrapper around the background agent task.
+
+        When multiplexing is active, resolve the inbound source's profile and
+        run the whole task inside ``_profile_runtime_scope`` so credentials
+        resolve from that profile's secret scope. Mirrors the pattern in
+        ``_run_agent``.
+        """
+        if not getattr(getattr(self, "config", None), "multiplex_profiles", False):
+            return await self._run_background_task_inner(
+                prompt, source, task_id, event_message_id, media_urls, media_types,
+            )
+
+        profile_home = self._resolve_profile_home_for_source(source)
+        with _profile_runtime_scope(profile_home):
+            return await self._run_background_task_inner(
+                prompt, source, task_id, event_message_id, media_urls, media_types,
+            )
+
+    async def _run_background_task_inner(
+        self,
+        prompt: str,
+        source: "SessionSource",
+        task_id: str,
+        event_message_id: Optional[str] = None,
+        media_urls: Optional[List[str]] = None,
+        media_types: Optional[List[str]] = None,
     ) -> None:
         """Execute a background agent task and deliver the result to the chat."""
         from run_agent import AIAgent
diff --git a/tests/gateway/test_multiplex_background_task_scope.py b/tests/gateway/test_multiplex_background_task_scope.py
new file mode 100644
index 000000000000..891a37493ca3
--- /dev/null
+++ b/tests/gateway/test_multiplex_background_task_scope.py
@@ -0,0 +1,77 @@
+"""Regression: background tasks respect profile secret scope when multiplexing.
+
+Issue #60726: /background command runs _run_background_task without a profile
+scope, causing UnscopedSecretError when multiplexing is active and credentials
+are profile-scoped.
+"""
+import pytest
+from unittest import mock
+from pathlib import Path
+
+
+class TestBackgroundTaskProfileScope:
+    """_run_background_task installs _profile_runtime_scope when multiplexing is active."""
+
+    def test_background_task_calls_inner_wrapped_in_scope_when_multiplex_active(self):
+        """When multiplex_profiles is True, _run_background_task wraps call in _profile_runtime_scope."""
+        from gateway.run import GatewayRunner
+
+        config = {"multiplex_profiles": True}
+        gw = GatewayRunner(config=config)
+        gw._session_db = mock.MagicMock()
+        gw._adapter_for_source = mock.MagicMock(return_value=mock.MagicMock())
+
+        mock_inner = mock.AsyncMock(return_value=None)
+        gw._run_background_task_inner = mock_inner
+
+        import asyncio
+        source = mock.MagicMock()
+        source.profile = "test_profile"
+
+        # Mock _resolve_profile_home_for_source to return a known path
+        with mock.patch.object(gw, "_resolve_profile_home_for_source", return_value=Path("/fake/profile")):
+            # Mock _profile_runtime_scope
+            from gateway.run import _profile_runtime_scope
+            with mock.patch("gateway.run._profile_runtime_scope") as mock_scope:
+                mock_scope.return_value.__enter__ = mock.MagicMock()
+                mock_scope.return_value.__exit__ = mock.MagicMock()
+
+                asyncio.run(
+                    gw._run_background_task(
+                        prompt="test",
+                        source=source,
+                        task_id="test_task",
+                    )
+                )
+
+                # _profile_runtime_scope should have been called with profile_home (Path object)
+                mock_scope.assert_called_once_with(Path("/fake/profile"))
+                mock_inner.assert_called_once()
+
+    def test_background_task_calls_inner_direct_when_multiplex_disabled(self):
+        """When multiplex_profiles is False, _run_background_task calls inner directly."""
+        from gateway.run import GatewayRunner
+
+        config = {"multiplex_profiles": False}
+        gw = GatewayRunner(config=config)
+        gw._session_db = mock.MagicMock()
+        gw._adapter_for_source = mock.MagicMock(return_value=mock.MagicMock())
+
+        mock_inner = mock.AsyncMock(return_value=None)
+        gw._run_background_task_inner = mock_inner
+
+        import asyncio
+        source = mock.MagicMock()
+
+        with mock.patch("gateway.run._profile_runtime_scope") as mock_scope:
+            asyncio.run(
+                gw._run_background_task(
+                    prompt="test",
+                    source=source,
+                    task_id="test_task",
+                )
+            )
+
+            # _profile_runtime_scope should NOT have been called
+            mock_scope.assert_not_called()
+            mock_inner.assert_called_once()
\ No newline at end of file