diff --git a/homeassistant/components/cover/services.yaml b/homeassistant/components/cover/services.yaml
index 2f8e20464f3f..8ab42c6d3e97 100644
--- a/homeassistant/components/cover/services.yaml
+++ b/homeassistant/components/cover/services.yaml
@@ -6,6 +6,8 @@ open_cover:
   target:
     entity:
       domain: cover
+      supported_features:
+        - cover.CoverEntityFeature.OPEN
 
 close_cover:
   name: Close
@@ -13,6 +15,8 @@ close_cover:
   target:
     entity:
       domain: cover
+      supported_features:
+        - cover.CoverEntityFeature.CLOSE
 
 toggle:
   name: Toggle
@@ -20,6 +24,9 @@ toggle:
   target:
     entity:
       domain: cover
+      supported_features:
+        - - cover.CoverEntityFeature.CLOSE
+          - cover.CoverEntityFeature.OPEN
 
 set_cover_position:
   name: Set position
@@ -27,6 +34,8 @@ set_cover_position:
   target:
     entity:
       domain: cover
+      supported_features:
+        - cover.CoverEntityFeature.SET_POSITION
   fields:
     position:
       name: Position
@@ -44,6 +53,8 @@ stop_cover:
   target:
     entity:
       domain: cover
+      supported_features:
+        - cover.CoverEntityFeature.STOP
 
 open_cover_tilt:
   name: Open tilt
@@ -51,6 +62,8 @@ open_cover_tilt:
   target:
     entity:
       domain: cover
+      supported_features:
+        - cover.CoverEntityFeature.OPEN_TILT
 
 close_cover_tilt:
   name: Close tilt
@@ -58,6 +71,8 @@ close_cover_tilt:
   target:
     entity:
       domain: cover
+      supported_features:
+        - cover.CoverEntityFeature.CLOSE_TILT
 
 toggle_cover_tilt:
   name: Toggle tilt
@@ -65,6 +80,9 @@ toggle_cover_tilt:
   target:
     entity:
       domain: cover
+      supported_features:
+        - - cover.CoverEntityFeature.CLOSE_TILT
+          - cover.CoverEntityFeature.OPEN_TILT
 
 set_cover_tilt_position:
   name: Set tilt position
@@ -72,6 +90,8 @@ set_cover_tilt_position:
   target:
     entity:
       domain: cover
+      supported_features:
+        - cover.CoverEntityFeature.SET_TILT_POSITION
   fields:
     tilt_position:
       name: Tilt position
@@ -89,3 +109,5 @@ stop_cover_tilt:
   target:
     entity:
       domain: cover
+      supported_features:
+        - cover.CoverEntityFeature.STOP_TILT
diff --git a/homeassistant/helpers/selector.py b/homeassistant/helpers/selector.py
index 84c0f769c7ce..abd4d2e623ee 100644
--- a/homeassistant/helpers/selector.py
+++ b/homeassistant/helpers/selector.py
@@ -122,12 +122,9 @@ def _entity_features() -> dict[str, type[IntFlag]]:
     }
 
 
-def _validate_supported_feature(supported_feature: int | str) -> int:
+def _validate_supported_feature(supported_feature: str) -> int:
     """Validate a supported feature and resolve an enum string to its value."""
 
-    if isinstance(supported_feature, int):
-        return supported_feature
-
     known_entity_features = _entity_features()
 
     try:
@@ -144,6 +141,20 @@ def _validate_supported_feature(supported_feature: int | str) -> int:
         raise vol.Invalid(f"Unknown supported feature '{supported_feature}'") from exc
 
 
+def _validate_supported_features(supported_features: int | list[str]) -> int:
+    """Validate a supported feature and resolve an enum string to its value."""
+
+    if isinstance(supported_features, int):
+        return supported_features
+
+    feature_mask = 0
+
+    for supported_feature in supported_features:
+        feature_mask |= _validate_supported_feature(supported_feature)
+
+    return feature_mask
+
+
 ENTITY_FILTER_SELECTOR_CONFIG_SCHEMA = vol.Schema(
     {
         # Integration that provided the entity
@@ -153,7 +164,9 @@ ENTITY_FILTER_SELECTOR_CONFIG_SCHEMA = vol.Schema(
         # Device class of the entity
         vol.Optional("device_class"): vol.All(cv.ensure_list, [str]),
         # Features supported by the entity
-        vol.Optional("supported_features"): [vol.All(str, _validate_supported_feature)],
+        vol.Optional("supported_features"): [
+            vol.All(cv.ensure_list, [str], _validate_supported_features)
+        ],
     }
 )
 
diff --git a/tests/helpers/test_selector.py b/tests/helpers/test_selector.py
index c518ad227a76..fd2dba4b0845 100644
--- a/tests/helpers/test_selector.py
+++ b/tests/helpers/test_selector.py
@@ -235,6 +235,22 @@ def test_device_selector_schema(schema, valid_selections, invalid_selections) ->
             ("light.abc123", "blah.blah", FAKE_UUID),
             (None,),
         ),
+        (
+            {
+                "filter": [
+                    {
+                        "supported_features": [
+                            [
+                                "light.LightEntityFeature.EFFECT",
+                                "light.LightEntityFeature.TRANSITION",
+                            ]
+                        ]
+                    },
+                ]
+            },
+            ("light.abc123", "blah.blah", FAKE_UUID),
+            (None,),
+        ),
         (
             {
                 "filter": [