diff --git a/synapse/handlers/sliding_sync.py b/synapse/handlers/sliding_sync.py
index 1c2ed95660..b108e8a4a2 100644
--- a/synapse/handlers/sliding_sync.py
+++ b/synapse/handlers/sliding_sync.py
@@ -1807,7 +1807,7 @@ class SlidingSyncHandler:
         """
 
         user_id = sync_config.user.to_string()
-        device_id = sync_config.device_id
+        device_id = sync_config.requester.device_id
 
         # Check that this request has a valid device ID (not all requests have
         # to belong to a device, and so device_id is None), and that the
diff --git a/synapse/rest/client/sync.py b/synapse/rest/client/sync.py
index b3967db18d..2909052bbf 100644
--- a/synapse/rest/client/sync.py
+++ b/synapse/rest/client/sync.py
@@ -881,7 +881,6 @@ class SlidingSyncRestServlet(RestServlet):
         )
 
         user = requester.user
-        device_id = requester.device_id
 
         timeout = parse_integer(request, "timeout", default=0)
         # Position in the stream
@@ -902,11 +901,12 @@ class SlidingSyncRestServlet(RestServlet):
 
         sync_config = SlidingSyncConfig(
             user=user,
-            device_id=device_id,
+            requester=requester,
             # FIXME: Currently, we're just manually copying the fields from the
-            # `SlidingSyncBody` into the config. How can we gurantee into the future
+            # `SlidingSyncBody` into the config. How can we guarantee into the future
             # that we don't forget any? I would like something more structured like
             # `copy_attributes(from=body, to=config)`
+            conn_id=body.conn_id,
             lists=body.lists,
             room_subscriptions=body.room_subscriptions,
             extensions=body.extensions,
diff --git a/synapse/types/handlers/__init__.py b/synapse/types/handlers/__init__.py
index 642e5483a9..0c2ab13c93 100644
--- a/synapse/types/handlers/__init__.py
+++ b/synapse/types/handlers/__init__.py
@@ -34,6 +34,7 @@ from synapse.events import EventBase
 from synapse.types import (
     JsonDict,
     JsonMapping,
+    Requester,
     SlidingSyncStreamToken,
     StreamToken,
     UserID,
@@ -108,7 +109,7 @@ class SlidingSyncConfig(SlidingSyncBody):
     """
 
     user: UserID
-    device_id: Optional[str]
+    requester: Requester
 
     # Pydantic config
     class Config:
@@ -119,6 +120,31 @@ class SlidingSyncConfig(SlidingSyncBody):
         # Allow custom types like `UserID` to be used in the model
         arbitrary_types_allowed = True
 
+    def connection_id(self) -> str:
+        """Return a string identifier for this connection. May clash with
+        connection IDs from different users.
+
+        This is generally a combination of device ID and conn_id. However, both
+        these two are optional (e.g. puppet access tokens don't have device
+        IDs), so this handles those edge cases.
+        """
+
+        # `conn_id` can be null, in which case we default to the empty string
+        # (if conn ID is empty then the client can't have multiple sync loops)
+        conn_id = self.conn_id or ""
+
+        if self.requester.device_id:
+            return f"D/{self.requester.device_id}/{conn_id}"
+
+        if self.requester.access_token_id:
+            # If we don't have a device, then the access token ID should be a
+            # stable ID.
+            return f"A/{self.requester.access_token_id}/{conn_id}"
+
+        # If we have neither then its likely an AS or some weird token. Either
+        # way we can just fail here.
+        raise Exception("Cannot use sliding sync with access token type")
+
 
 class OperationType(Enum):
     """
diff --git a/synapse/types/rest/client/__init__.py b/synapse/types/rest/client/__init__.py
index dbe37bc712..5be8cf5389 100644
--- a/synapse/types/rest/client/__init__.py
+++ b/synapse/types/rest/client/__init__.py
@@ -120,6 +120,9 @@ class SlidingSyncBody(RequestBodyModel):
     Sliding Sync API request body.
 
     Attributes:
+        conn_id: An optional string to identify this connection to the server. If this
+            is missing, only 1 sliding sync connection can be made to the server at
+            any one time.
         lists: Sliding window API. A map of list key to list information
             (:class:`SlidingSyncList`). Max lists: 100. The list keys should be
             arbitrary strings which the client is using to refer to the list. Keep this
@@ -315,6 +318,8 @@ class SlidingSyncBody(RequestBodyModel):
 
         to_device: Optional[ToDeviceExtension] = None
 
+    conn_id: Optional[str]
+
     # mypy workaround via https://github.com/pydantic/pydantic/issues/156#issuecomment-1130883884
     if TYPE_CHECKING:
         lists: Optional[Dict[str, SlidingSyncList]] = None