diff --git a/changelog.d/10887.bugfix b/changelog.d/10887.bugfix
new file mode 100644
index 000000000000..2d1f67489a89
--- /dev/null
+++ b/changelog.d/10887.bugfix
@@ -0,0 +1 @@
+Allow the `.` and `~` characters when creating registration tokens as per the change to [MSC3231](https://github.com/matrix-org/matrix-doc/pull/3231).
diff --git a/synapse/rest/admin/registration_tokens.py b/synapse/rest/admin/registration_tokens.py
index 5a1c929d85c4..aba48f6e7bab 100644
--- a/synapse/rest/admin/registration_tokens.py
+++ b/synapse/rest/admin/registration_tokens.py
@@ -113,7 +113,7 @@ def __init__(self, hs: "HomeServer"):
         self.store = hs.get_datastore()
         self.clock = hs.get_clock()
         # A string of all the characters allowed to be in a registration_token
-        self.allowed_chars = string.ascii_letters + string.digits + "-_"
+        self.allowed_chars = string.ascii_letters + string.digits + "._~-"
         self.allowed_chars_set = set(self.allowed_chars)
 
     async def on_POST(self, request: SynapseRequest) -> Tuple[int, JsonDict]:
diff --git a/tests/rest/admin/test_registration_tokens.py b/tests/rest/admin/test_registration_tokens.py
index 4927321e5a4f..9bac423ae048 100644
--- a/tests/rest/admin/test_registration_tokens.py
+++ b/tests/rest/admin/test_registration_tokens.py
@@ -95,8 +95,10 @@ def test_create_using_defaults(self):
 
     def test_create_specifying_fields(self):
         """Create a token specifying the value of all fields."""
+        # As many of the allowed characters as possible with length <= 64
+        token = "adefghijklmnopqrstuvwxyzABCDEFGHIJKLMNOPQRSTUVWXYZ0123456789._~-"
         data = {
-            "token": "abcd",
+            "token": token,
             "uses_allowed": 1,
             "expiry_time": self.clock.time_msec() + 1000000,
         }
@@ -109,7 +111,7 @@ def test_create_specifying_fields(self):
         )
 
         self.assertEqual(200, int(channel.result["code"]), msg=channel.result["body"])
-        self.assertEqual(channel.json_body["token"], "abcd")
+        self.assertEqual(channel.json_body["token"], token)
         self.assertEqual(channel.json_body["uses_allowed"], 1)
         self.assertEqual(channel.json_body["expiry_time"], data["expiry_time"])
         self.assertEqual(channel.json_body["pending"], 0)
@@ -193,7 +195,7 @@ def test_create_unable_to_generate_token(self):
         """Check right error is raised when server can't generate unique token."""
         # Create all possible single character tokens
         tokens = []
-        for c in string.ascii_letters + string.digits + "-_":
+        for c in string.ascii_letters + string.digits + "._~-":
             tokens.append(
                 {
                     "token": c,