diff --git a/changelogs/fragments/81666-handlers-run_once.yml b/changelogs/fragments/81666-handlers-run_once.yml
new file mode 100644
index 00000000000..e5cac9e2161
--- /dev/null
+++ b/changelogs/fragments/81666-handlers-run_once.yml
@@ -0,0 +1,2 @@
+bugfixes:
+  - Fix ``run_once`` being incorrectly interpreted on handlers (https://github.com/ansible/ansible/issues/81666)
diff --git a/lib/ansible/playbook/handler.py b/lib/ansible/playbook/handler.py
index 68970b4f1f0..2f2839813a7 100644
--- a/lib/ansible/playbook/handler.py
+++ b/lib/ansible/playbook/handler.py
@@ -53,6 +53,9 @@ class Handler(Task):
     def remove_host(self, host):
         self.notified_hosts = [h for h in self.notified_hosts if h != host]
 
+    def clear_hosts(self):
+        self.notified_hosts = []
+
     def is_host_notified(self, host):
         return host in self.notified_hosts
 
diff --git a/lib/ansible/plugins/strategy/__init__.py b/lib/ansible/plugins/strategy/__init__.py
index eda0e0af62e..d471effa2c3 100644
--- a/lib/ansible/plugins/strategy/__init__.py
+++ b/lib/ansible/plugins/strategy/__init__.py
@@ -800,10 +800,6 @@ class StrategyBase:
 
             ret_results.append(task_result)
 
-            if isinstance(original_task, Handler):
-                for handler in (h for b in iterator._play.handlers for h in b.block if h._uuid == original_task._uuid):
-                    handler.remove_host(original_host)
-
             if one_pass or max_passes is not None and (cur_pass + 1) >= max_passes:
                 break
 
@@ -1091,9 +1087,6 @@ class StrategyBase:
             header = skip_reason if skipped else msg
             display.vv(f"META: {header}")
 
-        if isinstance(task, Handler):
-            task.remove_host(target_host)
-
         res = TaskResult(target_host, task, result)
         if skipped:
             self._tqm.send_callback('v2_runner_on_skipped', res)
diff --git a/lib/ansible/plugins/strategy/free.py b/lib/ansible/plugins/strategy/free.py
index fe6ad7df46f..82a21b1c3c1 100644
--- a/lib/ansible/plugins/strategy/free.py
+++ b/lib/ansible/plugins/strategy/free.py
@@ -146,6 +146,8 @@ class StrategyModule(StrategyBase):
                         # advance the host, mark the host blocked, and queue it
                         self._blocked_hosts[host_name] = True
                         iterator.set_state_for_host(host.name, state)
+                        if isinstance(task, Handler):
+                            task.remove_host(host)
 
                         try:
                             action = action_loader.get(task.action, class_only=True, collection_list=task.collections)
diff --git a/lib/ansible/plugins/strategy/linear.py b/lib/ansible/plugins/strategy/linear.py
index 8ab3e3d5313..2fd4cbae3c2 100644
--- a/lib/ansible/plugins/strategy/linear.py
+++ b/lib/ansible/plugins/strategy/linear.py
@@ -242,6 +242,12 @@ class StrategyModule(StrategyBase):
                         self._queue_task(host, task, task_vars, play_context)
                         del task_vars
 
+                    if isinstance(task, Handler):
+                        if run_once:
+                            task.clear_hosts()
+                        else:
+                            task.remove_host(host)
+
                     # if we're bypassing the host loop, break out now
                     if run_once:
                         break
diff --git a/test/integration/targets/handlers/runme.sh b/test/integration/targets/handlers/runme.sh
index 9b17dc7bbf3..757200de385 100755
--- a/test/integration/targets/handlers/runme.sh
+++ b/test/integration/targets/handlers/runme.sh
@@ -195,3 +195,6 @@ ansible localhost -m include_role -a "name=r1-dep_chain-vars" "$@"
 
 ansible-playbook test_include_tasks_in_include_role.yml "$@" 2>&1 | tee out.txt
 [ "$(grep out.txt -ce 'handler ran')" = "1" ]
+
+ansible-playbook test_run_once.yml -i inventory.handlers "$@" 2>&1 | tee out.txt
+[ "$(grep out.txt -ce 'handler ran once')" = "1" ]
diff --git a/test/integration/targets/handlers/test_run_once.yml b/test/integration/targets/handlers/test_run_once.yml
new file mode 100644
index 00000000000..5418b46a6ff
--- /dev/null
+++ b/test/integration/targets/handlers/test_run_once.yml
@@ -0,0 +1,10 @@
+- hosts: A,B,C
+  gather_facts: false
+  tasks:
+    - command: echo
+      notify: handler
+  handlers:
+    - name: handler
+      run_once: true
+      debug:
+        msg: handler ran once