diff --git a/changelog.d/10815.misc b/changelog.d/10815.misc
new file mode 100644
index 000000000000..fc2534dc14be
--- /dev/null
+++ b/changelog.d/10815.misc
@@ -0,0 +1 @@
+Specify the type of token in generic "Invalid token" error messages.
\ No newline at end of file
diff --git a/synapse/handlers/auth.py b/synapse/handlers/auth.py
index fbbf6fd834c4..3ea627008314 100644
--- a/synapse/handlers/auth.py
+++ b/synapse/handlers/auth.py
@@ -1347,7 +1347,7 @@ async def validate_short_term_login_token(
         try:
             res = self.macaroon_gen.verify_short_term_login_token(login_token)
         except Exception:
-            raise AuthError(403, "Invalid token", errcode=Codes.FORBIDDEN)
+            raise AuthError(403, "Invalid login token", errcode=Codes.FORBIDDEN)
 
         await self.auth.check_auth_blocking(res.user_id)
         return res
diff --git a/synapse/storage/relations.py b/synapse/storage/relations.py
index c552dbf04c8e..10a46b5e82ed 100644
--- a/synapse/storage/relations.py
+++ b/synapse/storage/relations.py
@@ -73,7 +73,7 @@ def from_string(string: str) -> "RelationPaginationToken":
             t, s = string.split("-")
             return RelationPaginationToken(int(t), int(s))
         except ValueError:
-            raise SynapseError(400, "Invalid token")
+            raise SynapseError(400, "Invalid relation pagination token")
 
     def to_string(self) -> str:
         return "%d-%d" % (self.topological, self.stream)
@@ -103,7 +103,7 @@ def from_string(string: str) -> "AggregationPaginationToken":
             c, s = string.split("-")
             return AggregationPaginationToken(int(c), int(s))
         except ValueError:
-            raise SynapseError(400, "Invalid token")
+            raise SynapseError(400, "Invalid aggregation pagination token")
 
     def to_string(self) -> str:
         return "%d-%d" % (self.count, self.stream)
diff --git a/synapse/types.py b/synapse/types.py
index d4759b2dfd45..90168ce8fab3 100644
--- a/synapse/types.py
+++ b/synapse/types.py
@@ -511,7 +511,7 @@ async def parse(cls, store: "DataStore", string: str) -> "RoomStreamToken":
                 )
         except Exception:
             pass
-        raise SynapseError(400, "Invalid token %r" % (string,))
+        raise SynapseError(400, "Invalid room stream token %r" % (string,))
 
     @classmethod
     def parse_stream_token(cls, string: str) -> "RoomStreamToken":
@@ -520,7 +520,7 @@ def parse_stream_token(cls, string: str) -> "RoomStreamToken":
                 return cls(topological=None, stream=int(string[1:]))
         except Exception:
             pass
-        raise SynapseError(400, "Invalid token %r" % (string,))
+        raise SynapseError(400, "Invalid room stream token %r" % (string,))
 
     def copy_and_advance(self, other: "RoomStreamToken") -> "RoomStreamToken":
         """Return a new token such that if an event is after both this token and
@@ -619,7 +619,7 @@ async def from_string(cls, store: "DataStore", string: str) -> "StreamToken":
                 await RoomStreamToken.parse(store, keys[0]), *(int(k) for k in keys[1:])
             )
         except Exception:
-            raise SynapseError(400, "Invalid Token")
+            raise SynapseError(400, "Invalid stream token")
 
     async def to_string(self, store: "DataStore") -> str:
         return self._SEPARATOR.join(