diff --git a/synapse/appservice/__init__.py b/synapse/appservice/__init__.py
index 6ee5240c4e..64a8605652 100644
--- a/synapse/appservice/__init__.py
+++ b/synapse/appservice/__init__.py
@@ -85,7 +85,8 @@ class ApplicationService:
         protocols: Optional[Iterable[str]] = None,
         rate_limited: bool = True,
         ip_range_whitelist: Optional[IPSet] = None,
-        supports_ephemeral: bool = False,
+        receive_ephemeral: bool = False,
+        msc2409_push_ephemeral: bool = False,
         msc3202_transaction_extensions: bool = False,
         msc4190_device_management: bool = False,
     ):
@@ -99,7 +100,8 @@ class ApplicationService:
         self.namespaces = self._check_namespaces(namespaces)
         self.id = id
         self.ip_range_whitelist = ip_range_whitelist
-        self.supports_ephemeral = supports_ephemeral
+        self.receive_ephemeral = receive_ephemeral
+        self.msc2409_push_ephemeral = msc2409_push_ephemeral
         self.msc3202_transaction_extensions = msc3202_transaction_extensions
         self.msc4190_device_management = msc4190_device_management
 
diff --git a/synapse/appservice/api.py b/synapse/appservice/api.py
index 19322471dc..f4992bdf5c 100644
--- a/synapse/appservice/api.py
+++ b/synapse/appservice/api.py
@@ -350,7 +350,7 @@ class ApplicationServiceApi(SimpleHttpClient):
 
         # Never send ephemeral events to appservices that do not support it
         body: JsonDict = {"events": serialized_events}
-        if service.supports_ephemeral:
+        if service.msc2409_push_ephemeral:
             body.update(
                 {
                     # TODO: Update to stable prefixes once MSC2409 completes FCP merge.
@@ -359,6 +359,13 @@ class ApplicationServiceApi(SimpleHttpClient):
                 }
             )
 
+        if service.receive_ephemeral:
+            body.update(
+                {
+                    "ephemeral": ephemeral,
+                }
+            )
+
         # TODO: Update to stable prefixes once MSC3202 completes FCP merge
         if service.msc3202_transaction_extensions:
             if one_time_keys_count:
diff --git a/synapse/config/appservice.py b/synapse/config/appservice.py
index dda6bcd1b7..6ce2c18a2b 100644
--- a/synapse/config/appservice.py
+++ b/synapse/config/appservice.py
@@ -170,7 +170,19 @@ def _load_appservice(
     if as_info.get("ip_range_whitelist"):
         ip_range_whitelist = IPSet(as_info.get("ip_range_whitelist"))
 
-    supports_ephemeral = as_info.get("de.sorunome.msc2409.push_ephemeral", False)
+    unstable_msc2409_supports_ephemeral = as_info.get(
+        "de.sorunome.msc2409.push_ephemeral", False
+    )
+    if not isinstance(unstable_msc2409_supports_ephemeral, bool):
+        raise ValueError(
+            "The `de.sorunome.msc2409.push_ephemeral` option should be true or false if specified."
+        )
+
+    receive_ephemeral = as_info.get("receive_ephemeral", False)
+    if not isinstance(receive_ephemeral, bool):
+        raise ValueError(
+            "The `receive_ephemeral` option should be true or false if specified."
+        )
 
     # Opt-in flag for the MSC3202-specific transactional behaviour.
     # When enabled, appservice transactions contain the following information:
@@ -205,7 +217,8 @@ def _load_appservice(
         protocols=protocols,
         rate_limited=rate_limited,
         ip_range_whitelist=ip_range_whitelist,
-        supports_ephemeral=supports_ephemeral,
+        receive_ephemeral=receive_ephemeral,
+        msc2409_push_ephemeral=unstable_msc2409_supports_ephemeral,
         msc3202_transaction_extensions=msc3202_transaction_extensions,
         msc4190_device_management=msc4190_enabled,
     )
diff --git a/synapse/handlers/appservice.py b/synapse/handlers/appservice.py
index b7d1033351..fdb47ed839 100644
--- a/synapse/handlers/appservice.py
+++ b/synapse/handlers/appservice.py
@@ -300,9 +300,13 @@ class ApplicationServicesHandler:
                     StreamKeyType.TYPING,
                     StreamKeyType.RECEIPT,
                     StreamKeyType.PRESENCE,
-                    StreamKeyType.TO_DEVICE,
                 )
-                and service.supports_ephemeral
+                and (service.receive_ephemeral or service.msc2409_push_ephemeral)
+            )
+            # A previous version of MSC2409 supported sending to-device messages
+            # to the appservice, but this was removed in the stable version.
+            or (
+                stream_key == StreamKeyType.TO_DEVICE and service.msc2409_push_ephemeral
             )
             or (
                 stream_key == StreamKeyType.DEVICE_LIST
diff --git a/tests/handlers/test_appservice.py b/tests/handlers/test_appservice.py
index 1db630e9e4..f714abc122 100644
--- a/tests/handlers/test_appservice.py
+++ b/tests/handlers/test_appservice.py
@@ -1012,7 +1012,7 @@ class ApplicationServicesHandlerSendEventsTestCase(unittest.HomeserverTestCase):
             sender="@as:example.com",
             rate_limited=False,
             namespaces=namespaces,
-            supports_ephemeral=True,
+            receive_ephemeral=True,
         )
 
         # Register the application service
@@ -1097,7 +1097,7 @@ class ApplicationServicesHandlerDeviceListsTestCase(unittest.HomeserverTestCase)
                     }
                 ],
             },
-            supports_ephemeral=True,
+            receive_ephemeral=True,
             msc3202_transaction_extensions=as_supports_txn_extensions,
             # Must be set for Synapse to try pushing data to the AS
             hs_token="abcde",