diff --git a/synapse/rest/admin/registration_tokens.py b/synapse/rest/admin/registration_tokens.py
index e3aff93ae17a..eabdcd466d3a 100644
--- a/synapse/rest/admin/registration_tokens.py
+++ b/synapse/rest/admin/registration_tokens.py
@@ -176,7 +176,34 @@ async def on_POST(self, request: SynapseRequest) -> Tuple[int, JsonDict]:
                 400, "expiry_time must not be in the past", Codes.INVALID_PARAM
             )
 
-        await self.store.create_registration_token(token, uses_allowed, expiry_time)
+        created = await self.store.create_registration_token(
+            token, uses_allowed, expiry_time
+        )
+
+        if "token" not in body:
+            # The token was generated. If it could not be created because
+            # that token already exists, then try a few more times before
+            # reporting a failure.
+            i = 0
+            while not created and i < 3:
+                token = "".join(random.choices(self.allowed_chars, k=length))
+                created = await self.store.create_registration_token(
+                    token, uses_allowed, expiry_time
+                )
+                i += 1
+            if not created:
+                raise SynapseError(
+                    500,
+                    "The generated token already exists. Try again with a greater length.",
+                    Codes.UNKNOWN,
+                )
+
+        elif not created:
+            # The token was specified in the request, but it already exists
+            # so could not be created.
+            raise SynapseError(
+                400, f"Token already exists: {token}", Codes.INVALID_PARAM
+            )
 
         resp = {
             "token": token,
diff --git a/synapse/storage/databases/main/registration.py b/synapse/storage/databases/main/registration.py
index 4f09ba649cb2..b7df9bce22b8 100644
--- a/synapse/storage/databases/main/registration.py
+++ b/synapse/storage/databases/main/registration.py
@@ -1328,7 +1328,7 @@ async def get_one_registration_token(self, token: str) -> Optional[Dict[str, Any
 
     async def create_registration_token(
         self, token: str, uses_allowed: Optional[int], expiry_time: Optional[int]
-    ) -> None:
+    ) -> bool:
         """Create a new registration token. Used by the admin API.
 
         Args:
@@ -1354,9 +1354,8 @@ def _create_registration_token_txn(txn):
             )
 
             if row is not None:
-                raise SynapseError(
-                    400, f"Token already exists: {token}", Codes.INVALID_PARAM
-                )
+                # Token already exists
+                return False
 
             self.db_pool.simple_insert_txn(
                 txn,
@@ -1370,6 +1369,8 @@ def _create_registration_token_txn(txn):
                 },
             )
 
+            return True
+
         return await self.db_pool.runInteraction(
             "create_registration_token", _create_registration_token_txn
         )