diff --git a/src/functions/src/supabase_functions/_async/functions_client.py b/src/functions/src/supabase_functions/_async/functions_client.py
index 2f7529b1..b7a7edc2 100644
--- a/src/functions/src/supabase_functions/_async/functions_client.py
+++ b/src/functions/src/supabase_functions/_async/functions_client.py
@@ -95,6 +95,13 @@ async def _request(
                 method, str(url), json=json, headers=headers, params=params
             )
         )
+        # Relay failures set this header even on non-2xx responses.
+        if response.headers.get("x-relay-error") == "true":
+            raise FunctionsRelayError(
+                response.json().get("error")
+                or "Relay Error invoking the Edge Function",
+                response.status_code,
+            )
         try:
             response.raise_for_status()
         except HTTPError as exc:
@@ -165,10 +172,6 @@ async def invoke(
         response = await self._request(
             "POST", [function_name], headers=headers, json=body, params=params
         )
-        is_relay_error = response.headers.get("x-relay-header")
-
-        if is_relay_error and is_relay_error == "true":
-            raise FunctionsRelayError(response.json().get("error"))
 
         if response_type == "json":
             data = response.json()
diff --git a/src/functions/src/supabase_functions/_sync/functions_client.py b/src/functions/src/supabase_functions/_sync/functions_client.py
index 18f073d7..400814df 100644
--- a/src/functions/src/supabase_functions/_sync/functions_client.py
+++ b/src/functions/src/supabase_functions/_sync/functions_client.py
@@ -95,6 +95,13 @@ def _request(
                 method, str(url), json=json, headers=headers, params=params
             )
         )
+        # Relay failures set this header even on non-2xx responses.
+        if response.headers.get("x-relay-error") == "true":
+            raise FunctionsRelayError(
+                response.json().get("error")
+                or "Relay Error invoking the Edge Function",
+                response.status_code,
+            )
         try:
             response.raise_for_status()
         except HTTPError as exc:
@@ -165,10 +172,6 @@ def invoke(
         response = self._request(
             "POST", [function_name], headers=headers, json=body, params=params
         )
-        is_relay_error = response.headers.get("x-relay-header")
-
-        if is_relay_error and is_relay_error == "true":
-            raise FunctionsRelayError(response.json().get("error"))
 
         if response_type == "json":
             data = response.json()
diff --git a/src/functions/tests/_async/test_function_client.py b/src/functions/tests/_async/test_function_client.py
index a821deb8..f9d728b9 100644
--- a/src/functions/tests/_async/test_function_client.py
+++ b/src/functions/tests/_async/test_function_client.py
@@ -155,8 +155,9 @@ async def test_invoke_with_http_error(client: AsyncFunctionsClient) -> None:
 async def test_invoke_with_relay_error(client: AsyncFunctionsClient) -> None:
     mock_response = Mock(spec=Response)
     mock_response.json.return_value = {"error": "Relay error message"}
+    mock_response.status_code = 200
     mock_response.raise_for_status = Mock()
-    mock_response.headers = {"x-relay-header": "true"}
+    mock_response.headers = {"x-relay-error": "true"}
 
     with patch.object(
         client._client, "request", new_callable=AsyncMock
@@ -167,6 +168,29 @@ async def test_invoke_with_relay_error(client: AsyncFunctionsClient) -> None:
             await client.invoke("test-function")
 
 
+async def test_invoke_relay_error_on_non_2xx_status(
+    client: AsyncFunctionsClient,
+) -> None:
+    mock_response = Mock(spec=Response)
+    mock_response.json.return_value = {"error": "Relay error message"}
+    mock_response.status_code = 546
+    mock_response.raise_for_status.side_effect = HTTPError("HTTP Error")
+    mock_response.headers = {"x-relay-error": "true"}
+
+    with patch.object(
+        client._client, "request", new_callable=AsyncMock
+    ) as mock_request:
+        mock_request.return_value = mock_response
+
+        with pytest.raises(
+            FunctionsRelayError, match="Relay error message"
+        ) as exc_info:
+            await client.invoke("test-function")
+
+    assert not isinstance(exc_info.value, FunctionsHttpError)
+    assert exc_info.value.status == 546
+
+
 async def test_invoke_invalid_function_name(client: AsyncFunctionsClient) -> None:
     with pytest.raises(ValueError, match="function_name must a valid string value."):
         await client.invoke("")
diff --git a/src/functions/tests/_sync/test_function_client.py b/src/functions/tests/_sync/test_function_client.py
index 6be348df..e2cb1d83 100644
--- a/src/functions/tests/_sync/test_function_client.py
+++ b/src/functions/tests/_sync/test_function_client.py
@@ -145,8 +145,9 @@ def test_invoke_with_http_error(client: SyncFunctionsClient) -> None:
 def test_invoke_with_relay_error(client: SyncFunctionsClient) -> None:
     mock_response = Mock(spec=Response)
     mock_response.json.return_value = {"error": "Relay error message"}
+    mock_response.status_code = 200
     mock_response.raise_for_status = Mock()
-    mock_response.headers = {"x-relay-header": "true"}
+    mock_response.headers = {"x-relay-error": "true"}
 
     with patch.object(client._client, "request", new_callable=Mock) as mock_request:
         mock_request.return_value = mock_response
@@ -155,6 +156,25 @@ def test_invoke_with_relay_error(client: SyncFunctionsClient) -> None:
             client.invoke("test-function")
 
 
+def test_invoke_relay_error_on_non_2xx_status(client: SyncFunctionsClient) -> None:
+    mock_response = Mock(spec=Response)
+    mock_response.json.return_value = {"error": "Relay error message"}
+    mock_response.status_code = 546
+    mock_response.raise_for_status.side_effect = HTTPError("HTTP Error")
+    mock_response.headers = {"x-relay-error": "true"}
+
+    with patch.object(client._client, "request", new_callable=Mock) as mock_request:
+        mock_request.return_value = mock_response
+
+        with pytest.raises(
+            FunctionsRelayError, match="Relay error message"
+        ) as exc_info:
+            client.invoke("test-function")
+
+    assert not isinstance(exc_info.value, FunctionsHttpError)
+    assert exc_info.value.status == 546
+
+
 def test_invoke_invalid_function_name(client: SyncFunctionsClient) -> None:
     with pytest.raises(ValueError, match="function_name must a valid string value."):
         client.invoke("")