diff --git a/src/prompt_toolkit/application/application.py b/src/prompt_toolkit/application/application.py
index ecf52d176..aa94cc0ec 100644
--- a/src/prompt_toolkit/application/application.py
+++ b/src/prompt_toolkit/application/application.py
@@ -973,10 +973,12 @@ def _called_from_ipython() -> bool:
             # In Python 3.12, we can use asyncio.run(loop_factory=...)
             # For now, use `run_until_complete()`.
             loop = new_eventloop_with_inputhook(inputhook)
-            result = loop.run_until_complete(coro)
-            loop.run_until_complete(loop.shutdown_asyncgens())
-            loop.close()
-            return result
+            try:
+                result = loop.run_until_complete(coro)
+                loop.run_until_complete(loop.shutdown_asyncgens())
+                return result
+            finally:
+                loop.close()
 
         elif _called_from_ipython():
             # workaround to make input hooks work for IPython until
diff --git a/src/prompt_toolkit/eventloop/inputhook.py b/src/prompt_toolkit/eventloop/inputhook.py
index aaeb0cade..e19b16534 100644
--- a/src/prompt_toolkit/eventloop/inputhook.py
+++ b/src/prompt_toolkit/eventloop/inputhook.py
@@ -164,7 +164,12 @@ def input_is_ready() -> bool:
             #       should use `windll.kernel32.WaitForMultipleObjects`,
             #       because `select.select` can't wait for a pipe on Windows.
             if sys.platform != "win32":
-                select.select([self._r], [], [], None)
+                if hasattr(select, "poll"):
+                    poller = select.poll()
+                    poller.register(self._r, select.POLLIN)
+                    poller.poll()
+                else:
+                    select.select([self._r], [], [], None)
 
             os.read(self._r, 1024)
         except OSError:
@@ -182,7 +187,7 @@ def close(self) -> None:
         """
         Clean up resources.
         """
-        if self._r:
+        if self._r >= 0:
             os.close(self._r)
             os.close(self._w)
 
diff --git a/tests/test_inputhook.py b/tests/test_inputhook.py
new file mode 100644
index 000000000..4eaed9314
--- /dev/null
+++ b/tests/test_inputhook.py
@@ -0,0 +1,90 @@
+from __future__ import annotations
+
+import errno
+import os
+import selectors
+import sys
+import time
+from types import SimpleNamespace
+
+import pytest
+
+from prompt_toolkit.application import application
+from prompt_toolkit.eventloop import inputhook
+from prompt_toolkit.eventloop.inputhook import InputHookSelector
+from prompt_toolkit.input import create_pipe_input
+from prompt_toolkit.output import DummyOutput
+from prompt_toolkit.shortcuts import PromptSession
+
+
+def test_inputhook_selector_close_is_idempotent() -> None:
+    selector = InputHookSelector(selectors.DefaultSelector(), lambda context: None)
+
+    selector.close()
+    selector.close()
+
+
+@pytest.mark.skipif(
+    sys.platform == "win32" or not hasattr(inputhook.select, "poll"),
+    reason="requires POSIX poll support",
+)
+def test_inputhook_selector_supports_high_file_descriptors(monkeypatch) -> None:
+    # select.select() rejects descriptors >= FD_SETSIZE (usually 1024), even
+    # when the platform's default selector supports them.
+    fds: list[int] = []
+    selector: InputHookSelector | None = None
+    try:
+        try:
+            for _ in range(1050):
+                fds.append(os.open(os.devnull, os.O_RDONLY))
+        except OSError as e:
+            if e.errno == errno.EMFILE:
+                pytest.skip("not enough file descriptors to exercise FD_SETSIZE")
+            raise
+
+        selector = InputHookSelector(selectors.DefaultSelector(), lambda context: None)
+        if selector._r < 1024:
+            pytest.skip("the wake descriptor is below FD_SETSIZE")
+
+        monkeypatch.setattr(
+            inputhook,
+            "get_running_loop",
+            lambda: SimpleNamespace(_ready=[]),
+        )
+        assert selector.select(timeout=0) == []
+    finally:
+        if selector is not None:
+            selector.close()
+        for fd in fds:
+            os.close(fd)
+
+
+@pytest.mark.parametrize(
+    ("key", "exception"),
+    [("\x03", KeyboardInterrupt), ("\x04", EOFError)],
+)
+def test_application_closes_inputhook_loop_after_interrupt(
+    monkeypatch, key, exception
+) -> None:
+    loops = []
+    create_loop = application.new_eventloop_with_inputhook
+
+    def record_loop(input_hook):
+        loop = create_loop(input_hook)
+        loops.append(loop)
+        return loop
+
+    monkeypatch.setattr(application, "new_eventloop_with_inputhook", record_loop)
+
+    def wait_until_ready(context) -> None:
+        while not context.input_is_ready():
+            time.sleep(0.001)
+
+    with create_pipe_input() as pipe_input:
+        session = PromptSession(input=pipe_input, output=DummyOutput())
+        pipe_input.send_text(key)
+        with pytest.raises(exception):
+            session.prompt(inputhook=wait_until_ready)
+
+    assert len(loops) == 1
+    assert loops[0].is_closed()