diff --git a/changelog.d/16051.misc b/changelog.d/16051.misc
new file mode 100644
index 000000000000..1420d2eb3f36
--- /dev/null
+++ b/changelog.d/16051.misc
@@ -0,0 +1 @@
+Remove whole table locks on push rule modifications. Contributed by Nick @ Beeper (@fizzadar).
diff --git a/synapse/storage/databases/main/push_rule.py b/synapse/storage/databases/main/push_rule.py
index f72a23c58418..cf622e195cb6 100644
--- a/synapse/storage/databases/main/push_rule.py
+++ b/synapse/storage/databases/main/push_rule.py
@@ -449,26 +449,28 @@ def _add_push_rule_relative_txn(
         before: str,
         after: str,
     ) -> None:
-        # Lock the table since otherwise we'll have annoying races between the
-        # SELECT here and the UPSERT below.
-        self.database_engine.lock_table(txn, "push_rules")
-
         relative_to_rule = before or after
 
-        res = self.db_pool.simple_select_one_txn(
-            txn,
-            table="push_rules",
-            keyvalues={"user_name": user_id, "rule_id": relative_to_rule},
-            retcols=["priority_class", "priority"],
-            allow_none=True,
-        )
+        sql = """
+            SELECT priority, priority_class FROM push_rules
+            WHERE user_name = ? AND rule_id = ?
+        """
+
+        if isinstance(self.database_engine, PostgresEngine):
+            sql += " FOR UPDATE"
+        else:
+            # Annoyingly SQLite doesn't support row level locking, so lock the whole table
+            self.database_engine.lock_table(txn, "push_rules")
+
+        txn.execute(sql, (user_id, relative_to_rule))
+        row = txn.fetchone()
 
-        if not res:
+        if row is None:
             raise RuleNotFoundException(
                 "before/after rule not found: %s" % (relative_to_rule,)
             )
 
-        base_priority_class, base_rule_priority = res
+        base_rule_priority, base_priority_class = row
 
         if base_priority_class != priority_class:
             raise InconsistentRuleException(
@@ -516,9 +518,18 @@ def _add_push_rule_highest_priority_txn(
         conditions_json: str,
         actions_json: str,
     ) -> None:
-        # Lock the table since otherwise we'll have annoying races between the
-        # SELECT here and the UPSERT below.
-        self.database_engine.lock_table(txn, "push_rules")
+        if isinstance(self.database_engine, PostgresEngine):
+            # Postgres doesn't do FOR UPDATE on aggregate functions, so select the rows first
+            # then re-select the count/max below.
+            sql = """
+                SELECT * FROM push_rules
+                WHERE user_name = ? and priority_class = ?
+                FOR UPDATE
+            """
+            txn.execute(sql, (user_id, priority_class))
+        else:
+            # Annoyingly SQLite doesn't support row level locking, so lock the whole table
+            self.database_engine.lock_table(txn, "push_rules")
 
         # find the highest priority rule in that class
         sql = (