diff --git a/headroom/providers/registry.py b/headroom/providers/registry.py
index 04c212a4d..a8b816f3b 100644
--- a/headroom/providers/registry.py
+++ b/headroom/providers/registry.py
@@ -162,9 +162,27 @@ def resolve_extra_headers(
 
 def resolve_api_targets(overrides: ProviderApiOverrides) -> ProviderApiTargets:
     """Resolve normalized upstream provider targets from configured overrides."""
+    from headroom.copilot_auth import is_copilot_upstream_url
+
+    openai = _normalize_api_url(overrides.openai, default=DEFAULT_OPENAI_API_URL)
+
+    # GitHub Copilot serves BOTH its OpenAI surface (``/chat/completions``,
+    # ``/responses``) and its Anthropic surface (``/v1/messages``, for Claude
+    # models) from the same host. When the OpenAI target is a Copilot host
+    # (``wrap copilot --subscription`` / ``wrap vscode`` both point it there so
+    # GPT models work) but no Anthropic target was set, Claude-model requests
+    # fell back to ``DEFAULT_ANTHROPIC_API_URL`` (api.anthropic.com) and 401'd
+    # with the Copilot bearer — "Invalid bearer token" (#3247). Default the
+    # Anthropic target to the same Copilot host so those requests reach the
+    # surface that actually serves them. An explicit ``ANTHROPIC_TARGET_API_URL``
+    # still wins (only a ``None`` override is filled in here).
+    anthropic_override = overrides.anthropic
+    if anthropic_override is None and is_copilot_upstream_url(openai):
+        anthropic_override = openai
+
     return ProviderApiTargets(
-        anthropic=_normalize_api_url(overrides.anthropic, default=DEFAULT_ANTHROPIC_API_URL),
-        openai=_normalize_api_url(overrides.openai, default=DEFAULT_OPENAI_API_URL),
+        anthropic=_normalize_api_url(anthropic_override, default=DEFAULT_ANTHROPIC_API_URL),
+        openai=openai,
         gemini=_normalize_api_url(overrides.gemini, default=DEFAULT_GEMINI_API_URL),
         cloudcode=_normalize_api_url(overrides.cloudcode, default=DEFAULT_CLOUDCODE_API_URL),
         vertex=_normalize_api_url(overrides.vertex, default=DEFAULT_VERTEX_API_URL),
diff --git a/tests/test_provider_registry.py b/tests/test_provider_registry.py
index 0b0ff5b04..07310cd41 100644
--- a/tests/test_provider_registry.py
+++ b/tests/test_provider_registry.py
@@ -56,6 +56,55 @@ def test_resolve_api_targets_normalizes_trailing_v1() -> None:
     assert targets.vertex == "https://vertex.example"
 
 
+def test_copilot_openai_target_routes_anthropic_to_copilot() -> None:
+    """When the OpenAI target is a Copilot host and no Anthropic override is set,
+    the Anthropic target must default to the same Copilot host.
+
+    Copilot serves Claude models via its Anthropic surface (``/v1/messages``) on
+    the same host. Without this, Claude requests fell back to api.anthropic.com
+    and 401'd with the Copilot bearer ("Invalid bearer token", #3247).
+    """
+    targets = resolve_api_targets(
+        ProviderApiOverrides(
+            anthropic=None,
+            openai="https://api.githubcopilot.com",
+            gemini=None,
+            cloudcode=None,
+            vertex=None,
+        )
+    )
+    assert targets.openai == "https://api.githubcopilot.com"
+    assert targets.anthropic == "https://api.githubcopilot.com"
+
+
+def test_explicit_anthropic_override_wins_over_copilot_default() -> None:
+    """An explicit Anthropic target is never overridden by the Copilot default."""
+    targets = resolve_api_targets(
+        ProviderApiOverrides(
+            anthropic="https://api.anthropic.com",
+            openai="https://api.githubcopilot.com",
+            gemini=None,
+            cloudcode=None,
+            vertex=None,
+        )
+    )
+    assert targets.anthropic == "https://api.anthropic.com"
+
+
+def test_non_copilot_openai_target_leaves_anthropic_default() -> None:
+    """A non-Copilot OpenAI target must not touch the Anthropic default."""
+    targets = resolve_api_targets(
+        ProviderApiOverrides(
+            anthropic=None,
+            openai="https://api.openai.com",
+            gemini=None,
+            cloudcode=None,
+            vertex=None,
+        )
+    )
+    assert targets.anthropic == "https://api.anthropic.com"
+
+
 def test_proxy_config_exposes_provider_api_overrides() -> None:
     config = ProxyConfig(
         anthropic_api_url="https://anthropic.example",