diff --git a/python/copilot/client.py b/python/copilot/client.py
index ab3410a56c..e7026cab32 100644
--- a/python/copilot/client.py
+++ b/python/copilot/client.py
@@ -20,7 +20,6 @@
 import logging
 import os
 import re
-import shutil
 import subprocess
 import sys
 import threading
@@ -4328,11 +4327,15 @@ async def _start_cli_server(self) -> None:
         cli_path = conn.path
         assert cli_path is not None  # resolved in __init__
 
-        # Verify CLI exists
+        # Verify the resolved CLI path exists. `cli_path` must already come from
+        # an explicit override, COPILOT_CLI_PATH, or the SDK-managed downloaded
+        # runtime (see `_resolve_runtime_entrypoint`); the SDK never falls back to
+        # searching PATH for an arbitrary system installation.
         if not os.path.exists(cli_path):
-            original_path = cli_path
-            if (cli_path := shutil.which(cli_path)) is None:
-                raise RuntimeError(f"Copilot CLI not found at {original_path}")
+            raise RuntimeError(
+                f"Copilot CLI not found at {cli_path!r}. Set an explicit path, "
+                "COPILOT_CLI_PATH, or ensure the SDK-managed runtime download succeeded."
+            )
 
         # Start with user-provided args, then add SDK-managed args
         args = list(conn.args) + [
diff --git a/python/test_client.py b/python/test_client.py
index e62154e247..fff506ec99 100644
--- a/python/test_client.py
+++ b/python/test_client.py
@@ -80,6 +80,25 @@ def test_copilot_cli_path_does_not_require_runtime_bundle(tmp_path):
     assert connection.path == str(explicit)
 
 
+@pytest.mark.asyncio
+async def test_missing_cli_path_does_not_fall_back_to_path_search(tmp_path):
+    """A missing resolved CLI path must fail rather than silently resolving an
+    arbitrary same-named executable found on PATH (see #2524 / commit 05dd60e)."""
+    path_dir = tmp_path / "on_path"
+    path_dir.mkdir()
+    decoy = path_dir / "copilot"
+    decoy.write_text("#!/bin/sh\necho decoy\n")
+    decoy.chmod(0o755)
+
+    missing = tmp_path / "copilot"
+    connection = RuntimeConnection.for_stdio(path=str(missing))
+    client = CopilotClient(connection=connection, env={"PATH": str(path_dir)})
+
+    with patch.dict(os.environ, {"PATH": str(path_dir)}):
+        with pytest.raises(RuntimeError, match="Copilot CLI not found"):
+            await client._start_cli_server()
+
+
 class TestBuiltinPluginDirectories:
     @staticmethod
     async def _start_client(paths=None):