diff --git a/ansible_mitogen/runner.py b/ansible_mitogen/runner.py
index 44780aa2..45bb5f0b 100644
--- a/ansible_mitogen/runner.py
+++ b/ansible_mitogen/runner.py
@@ -38,6 +38,7 @@ how to build arguments for it, preseed related data, etc.
 from __future__ import absolute_import
 from __future__ import unicode_literals
 
+import atexit
 import ctypes
 import errno
 import imp
@@ -757,9 +758,25 @@ class NewStyleRunner(ScriptRunner):
         if klass and isinstance(exc, klass):
             mod.module.fail_json(**exc.results)
 
-    def _run(self):
-        code = self._get_code()
+    def _run_code(self, code, mod):
+        try:
+            if mitogen.core.PY3:
+                exec(code, vars(mod))
+            else:
+                exec('exec code in vars(mod)')
+        except Exception as e:
+            self._handle_magic_exception(mod, e)
+            raise
 
+    def _run_atexit_funcs(self):
+        """
+        Newer Ansibles use atexit.register() to trigger tmpdir cleanup, when
+        AnsibleModule.tmpdir is responsible for creating its own temporary
+        directory.
+        """
+        atexit._run_exitfuncs()
+
+    def _run(self):
         mod = types.ModuleType(self.main_module_name)
         mod.__package__ = None
         # Some Ansible modules use __file__ to find the Ansiballz temporary
@@ -771,16 +788,13 @@ class NewStyleRunner(ScriptRunner):
             'ansible_module_' + os.path.basename(self.path),
         )
 
+        code = self._get_code()
         exc = None
         try:
             try:
-                if mitogen.core.PY3:
-                    exec(code, vars(mod))
-                else:
-                    exec('exec code in vars(mod)')
-            except Exception as e:
-                self._handle_magic_exception(mod, e)
-                raise
+                self._run_code(code, mod)
+            finally:
+                self._run_atexit_funcs()
         except SystemExit as e:
             exc = e
 
diff --git a/tests/ansible/integration/runner/all.yml b/tests/ansible/integration/runner/all.yml
index 69c22edb..9dd209d7 100644
--- a/tests/ansible/integration/runner/all.yml
+++ b/tests/ansible/integration/runner/all.yml
@@ -1,3 +1,4 @@
+- import_playbook: atexit.yml
 - import_playbook: builtin_command_module.yml
 - import_playbook: custom_bash_hashbang_argument.yml
 - import_playbook: custom_bash_old_style_module.yml
@@ -15,6 +16,6 @@
 - import_playbook: environment_isolation.yml
 - import_playbook: etc_environment.yml
 - import_playbook: forking_active.yml
-- import_playbook: forking_inactive.yml
 - import_playbook: forking_correct_parent.yml
+- import_playbook: forking_inactive.yml
 - import_playbook: missing_module.yml
diff --git a/tests/ansible/integration/runner/atexit.yml b/tests/ansible/integration/runner/atexit.yml
new file mode 100644
index 00000000..872cdd57
--- /dev/null
+++ b/tests/ansible/integration/runner/atexit.yml
@@ -0,0 +1,31 @@
+# issue #397: newer Ansibles rely on atexit to cleanup their temporary
+# directories. Ensure atexit handlers run during runner completion.
+
+- name: integration/runner/atexit.yml
+  hosts: test-targets
+  gather_facts: false
+  any_errors_fatal: false
+  tasks:
+
+    #
+    # Verify a run with a healthy atexit handler. Broken handlers cause an
+    # exception to be raised.
+    #
+
+    - custom_python_run_script:
+        script: |
+          import atexit
+          atexit.register(lambda:
+            open('/tmp/atexit-was-triggered', 'w').write('yep'))
+
+    - slurp:
+        path: /tmp/atexit-was-triggered
+      register: out
+
+    - assert:
+        that:
+        - out.content|b64decode == "yep"
+
+    - file:
+        path: /tmp/atexit-was-triggered
+        state: absent