diff --git a/agent/auxiliary_client.py b/agent/auxiliary_client.py
index 84ab7741982bc..b86f1fa5561c3 100644
--- a/agent/auxiliary_client.py
+++ b/agent/auxiliary_client.py
@@ -4465,6 +4465,26 @@ def _resolve_task_provider_model(
     resolved_model = model or cfg_model
     resolved_api_mode = cfg_api_mode
 
+    # When an explicit provider is given and no task-config api_mode override,
+    # fall back to the provider profile's declared api_mode. Without this,
+    # plugin providers that declare api_mode="anthropic_messages" (i.e. their
+    # upstream speaks the Anthropic Messages API, not OpenAI Chat Completions)
+    # silently land on the OpenAI-wire transport and 404 from
+    # `chat/completions` calls. The URL-suffix detection in
+    # `_endpoint_speaks_anthropic_messages` only catches /anthropic-suffixed
+    # gateways; it misses plain-base-URL Anthropic-API endpoints (e.g. local
+    # proxies on 127.0.0.1:PORT). Reading the profile here closes the gap so
+    # any provider plugin can declare api_mode and have it honored regardless
+    # of upstream URL shape.
+    if provider and not resolved_api_mode:
+        try:
+            from providers import get_provider_profile as _gpf_resolve
+            _profile = _gpf_resolve(provider)
+            if _profile and getattr(_profile, "api_mode", None):
+                resolved_api_mode = _profile.api_mode
+        except Exception:
+            pass
+
     # Convenience aliases for direct API-key endpoints that aren't first-class
     # providers (e.g. ``provider: openai`` → custom + api.openai.com/v1).
     # Applied to both explicit args and config-derived values. When the user
diff --git a/tests/agent/test_aux_resolver_api_mode.py b/tests/agent/test_aux_resolver_api_mode.py
new file mode 100644
index 0000000000000..fb23ec96c613d
--- /dev/null
+++ b/tests/agent/test_aux_resolver_api_mode.py
@@ -0,0 +1,45 @@
+"""Regression test for _resolve_task_provider_model consulting ProviderProfile.api_mode.
+
+When an explicit provider is given without a task-level api_mode override, the
+resolver must fall back to the provider profile's declared api_mode so plugin
+providers whose upstream speaks the Anthropic Messages API are wrapped with the
+correct transport regardless of base-URL shape. Task config still wins.
+"""
+
+from types import SimpleNamespace
+from unittest.mock import patch
+
+import agent.auxiliary_client as ac
+
+
+def test_resolver_falls_back_to_profile_api_mode():
+    prof = SimpleNamespace(api_mode="anthropic_messages")
+    with patch("providers.get_provider_profile", return_value=prof):
+        provider, model, base_url, api_key, api_mode = ac._resolve_task_provider_model(
+            provider="myplugin"
+        )
+    assert provider == "myplugin"
+    assert api_mode == "anthropic_messages"
+
+
+def test_task_config_api_mode_still_wins_over_profile():
+    prof = SimpleNamespace(api_mode="anthropic_messages")
+    with patch("providers.get_provider_profile", return_value=prof), \
+         patch.object(ac, "_get_auxiliary_task_config",
+                      return_value={"provider": "myplugin", "api_mode": "chat_completions"}):
+        # Explicit provider arg with explicit api_mode override would be cfg-driven;
+        # here we pass provider via task config so cfg_api_mode is set.
+        provider, model, base_url, api_key, api_mode = ac._resolve_task_provider_model(
+            task="compression"
+        )
+    # cfg_api_mode set -> resolver must NOT overwrite it with the profile value.
+    assert api_mode == "chat_completions"
+
+
+def test_resolver_no_profile_api_mode_leaves_none():
+    prof = SimpleNamespace(api_mode=None)
+    with patch("providers.get_provider_profile", return_value=prof):
+        provider, model, base_url, api_key, api_mode = ac._resolve_task_provider_model(
+            provider="plainplugin"
+        )
+    assert api_mode is None