diff --git a/homeassistant/components/api/__init__.py b/homeassistant/components/api/__init__.py
index b794b60b33d..ba71fb0def1 100644
--- a/homeassistant/components/api/__init__.py
+++ b/homeassistant/components/api/__init__.py
@@ -390,6 +390,27 @@ class APIDomainServicesView(HomeAssistantView):
             )
 
         context = self.context(request)
+        if not hass.services.has_service(domain, service):
+            raise HTTPBadRequest from ServiceNotFound(domain, service)
+
+        if response_requested := "return_response" in request.query:
+            if (
+                hass.services.supports_response(domain, service)
+                is ha.SupportsResponse.NONE
+            ):
+                return self.json_message(
+                    "Service does not support responses. Remove return_response from request.",
+                    HTTPStatus.BAD_REQUEST,
+                )
+        elif (
+            hass.services.supports_response(domain, service) is ha.SupportsResponse.ONLY
+        ):
+            return self.json_message(
+                "Service call requires responses but caller did not ask for responses. "
+                "Add ?return_response to query parameters.",
+                HTTPStatus.BAD_REQUEST,
+            )
+
         changed_states: list[json_fragment] = []
 
         @ha.callback
@@ -406,13 +427,14 @@ class APIDomainServicesView(HomeAssistantView):
 
         try:
             # shield the service call from cancellation on connection drop
-            await shield(
+            response = await shield(
                 hass.services.async_call(
                     domain,
                     service,
                     data,  # type: ignore[arg-type]
                     blocking=True,
                     context=context,
+                    return_response=response_requested,
                 )
             )
         except (vol.Invalid, ServiceNotFound) as ex:
@@ -420,6 +442,11 @@ class APIDomainServicesView(HomeAssistantView):
         finally:
             cancel_listen()
 
+        if response_requested:
+            return self.json(
+                {"changed_states": changed_states, "service_response": response}
+            )
+
         return self.json(changed_states)
 
 
diff --git a/tests/components/api/test_init.py b/tests/components/api/test_init.py
index c283aeb718e..abce262fd12 100644
--- a/tests/components/api/test_init.py
+++ b/tests/components/api/test_init.py
@@ -3,6 +3,7 @@
 import asyncio
 from http import HTTPStatus
 import json
+from typing import Any
 from unittest.mock import patch
 
 from aiohttp import ServerDisconnectedError, web
@@ -355,6 +356,67 @@ async def test_api_call_service_with_data(
     assert state["attributes"] == {"data": 1}
 
 
+SERVICE_DICT = {"changed_states": [], "service_response": {"foo": "bar"}}
+RESP_REQUIRED = {
+    "message": (
+        "Service call requires responses but caller did not ask for "
+        "responses. Add ?return_response to query parameters."
+    )
+}
+RESP_UNSUPPORTED = {
+    "message": "Service does not support responses. Remove return_response from request."
+}
+
+
+@pytest.mark.parametrize(
+    (
+        "supports_response",
+        "requested_response",
+        "expected_number_of_service_calls",
+        "expected_status",
+        "expected_response",
+    ),
+    [
+        (ha.SupportsResponse.ONLY, True, 1, HTTPStatus.OK, SERVICE_DICT),
+        (ha.SupportsResponse.ONLY, False, 0, HTTPStatus.BAD_REQUEST, RESP_REQUIRED),
+        (ha.SupportsResponse.OPTIONAL, True, 1, HTTPStatus.OK, SERVICE_DICT),
+        (ha.SupportsResponse.OPTIONAL, False, 1, HTTPStatus.OK, []),
+        (ha.SupportsResponse.NONE, True, 0, HTTPStatus.BAD_REQUEST, RESP_UNSUPPORTED),
+        (ha.SupportsResponse.NONE, False, 1, HTTPStatus.OK, []),
+    ],
+)
+async def test_api_call_service_returns_response_requested_response(
+    hass: HomeAssistant,
+    mock_api_client: TestClient,
+    supports_response: ha.SupportsResponse,
+    requested_response: bool,
+    expected_number_of_service_calls: int,
+    expected_status: int,
+    expected_response: Any,
+) -> None:
+    """Test if the API allows us to call a service."""
+    test_value = []
+
+    @ha.callback
+    def listener(service_call):
+        """Record that our service got called."""
+        test_value.append(1)
+        return {"foo": "bar"}
+
+    hass.services.async_register(
+        "test_domain", "test_service", listener, supports_response=supports_response
+    )
+
+    resp = await mock_api_client.post(
+        "/api/services/test_domain/test_service"
+        + ("?return_response" if requested_response else "")
+    )
+    assert resp.status == expected_status
+    await hass.async_block_till_done()
+    assert len(test_value) == expected_number_of_service_calls
+    assert await resp.json() == expected_response
+
+
 async def test_api_call_service_client_closed(
     hass: HomeAssistant, mock_api_client: TestClient
 ) -> None: