diff --git a/ops/testing.py b/ops/testing.py
index 2c4229be6..96439943c 100755
--- a/ops/testing.py
+++ b/ops/testing.py
@@ -2503,12 +2503,19 @@ def __init__(self, backend: _TestingModelBackend, container_root: pathlib.Path):
 
     def _handle_exec(self, command_prefix: List[str], handler: ExecHandler):
         prefix = tuple(command_prefix)
-        for idx, registered_handler in enumerate(self._exec_handlers):
+        inserted = False
+        for idx in range(len(self._exec_handlers)):
+            if inserted:
+                idx = idx + 1
+            registered_handler = self._exec_handlers[idx]
             if prefix == registered_handler[0]:
                 self._exec_handlers[idx] = (prefix, handler)
                 return
-        self._exec_handlers.append((prefix, handler))
-        self._exec_handlers.sort(key=lambda pair: len(pair[0]), reverse=True)
+            if not inserted and len(prefix) > len(registered_handler[0]):
+                self._exec_handlers.insert(idx, (prefix, handler))
+                inserted = True
+        if not inserted:
+            self._exec_handlers.append((prefix, handler))
 
     def _check_connection(self):
         if not self._backend._can_connect(self):
@@ -2871,6 +2878,7 @@ def remove_path(self, path: str, *, recursive: bool = False):
             file_path.unlink()
 
     def _find_exec_handler(self, command: List[str]) -> Optional[ExecHandler]:
+        print(self._exec_handlers)
         for command_prefix, handler in self._exec_handlers:
             if tuple(command[:len(command_prefix)]) == command_prefix:
                 return handler
diff --git a/test/test_testing.py b/test/test_testing.py
index 5a9816aa6..8b0dcee4c 100644
--- a/test/test_testing.py
+++ b/test/test_testing.py
@@ -19,6 +19,7 @@
 import inspect
 import io
 import ipaddress
+import itertools
 import os
 import pathlib
 import platform
@@ -5092,3 +5093,19 @@ def handler(args):
         self.assertEqual(args_history[-1].group, "test_group")
         self.assertEqual(args_history[-1].group_id, 4)
         self.assertDictEqual(args_history[-1].environment, {"foo": "hello", "foobar": "barfoo"})
+
+    def test_registration_order(self):
+        for n in range(7):
+            pebble = self.harness._backend._pebble_clients[self.container.name]
+            for prefix_lengths in itertools.product(range(1, n + 1), repeat=n):
+                pebble._exec_handlers = []
+                for idx, prefix_len in enumerate(prefix_lengths):
+                    self.harness.handle_exec(self.container, [str(idx)] * prefix_len, result=0)
+                handlers = pebble._exec_handlers
+                self.assertTrue(all(
+                    len(handlers[i][0]) >= len(handlers[i + 1][0])
+                    for i in range(len(handlers) - 1)))
+                self.assertEqual(len(handlers), len(prefix_lengths))
+                for idx, handler in enumerate(handlers):
+                    self.harness.handle_exec(self.container, handler[0], result=idx)
+                    self.assertEqual(handlers[idx][1](None), idx)