diff --git a/src/prompt_toolkit/application/application.py b/src/prompt_toolkit/application/application.py
index 5e9c6a997..26e8ed85a 100644
--- a/src/prompt_toolkit/application/application.py
+++ b/src/prompt_toolkit/application/application.py
@@ -416,7 +416,8 @@ def reset(self) -> None:
 
         self._background_tasks: set[Task[None]] = set()
 
-        self.renderer.reset()
+        if self.renderer.has_rendered:
+            self.renderer.reset()
         self.key_processor.reset()
         self.layout.reset()
         self.vi_state.reset()
@@ -750,7 +751,8 @@ def flush_input() -> None:
                         # _redraw has a good chance to fail if it calls widgets
                         # with bad code. Make sure to reset the renderer
                         # anyway.
-                        self.renderer.reset()
+                        if self.renderer.has_rendered:
+                            self.renderer.reset()
 
                         # Unset `is_running`, this ensures that possibly
                         # scheduled draws won't paint during the following
diff --git a/src/prompt_toolkit/renderer.py b/src/prompt_toolkit/renderer.py
index fcfde223e..f9a78e984 100644
--- a/src/prompt_toolkit/renderer.py
+++ b/src/prompt_toolkit/renderer.py
@@ -363,6 +363,7 @@ def __init__(
         self._mouse_support_enabled = False
         self._bracketed_paste_enabled = False
         self._cursor_key_mode_reset = False
+        self._has_rendered = False
 
         # Future set when we are waiting for a CPR flag.
         self._waiting_for_cpr_futures: deque[Future[None]] = deque()
@@ -428,6 +429,7 @@ def reset(self, _scroll: bool = False, leave_alternate_screen: bool = True) -> N
 
         # Flush output. `disable_mouse_support` needs to write to stdout.
         self.output.flush()
+        self._has_rendered = self._in_alternate_screen
 
     @property
     def last_rendered_screen(self) -> Screen | None:
@@ -437,6 +439,11 @@ def last_rendered_screen(self) -> Screen | None:
         """
         return self._last_screen
 
+    @property
+    def has_rendered(self) -> bool:
+        """Whether the renderer currently has terminal state to reset."""
+        return self._has_rendered
+
     @property
     def height_is_known(self) -> bool:
         """
@@ -598,6 +605,7 @@ def render(
                 won't print any changes to this part.
         """
         output = self.output
+        self._has_rendered = True
 
         # Enter alternate screen.
         if self.full_screen and not self._in_alternate_screen:
diff --git a/tests/test_application.py b/tests/test_application.py
new file mode 100644
index 000000000..3bbae6f05
--- /dev/null
+++ b/tests/test_application.py
@@ -0,0 +1,81 @@
+from __future__ import annotations
+
+import asyncio
+
+import pytest
+
+from prompt_toolkit.application import Application
+from prompt_toolkit.input import create_pipe_input
+from prompt_toolkit.output import DummyOutput
+from prompt_toolkit.renderer import Renderer
+
+
+def test_renderer_is_not_reset_repeatedly_during_application_lifecycle(
+    monkeypatch,
+) -> None:
+    reset_calls = 0
+    reset_calls_before_render: list[int] = []
+    original_reset = Renderer.reset
+
+    def reset(self: Renderer, *args: object, **kwargs: object) -> None:
+        nonlocal reset_calls
+        reset_calls += 1
+        original_reset(self, *args, **kwargs)
+
+    monkeypatch.setattr(Renderer, "reset", reset)
+
+    with create_pipe_input() as input:
+        app: Application[None] = Application(
+            input=input,
+            output=DummyOutput(),
+            before_render=lambda _: reset_calls_before_render.append(reset_calls),
+        )
+        app.run(pre_run=lambda: app.exit())
+
+    assert reset_calls_before_render == [1, 1]
+    assert reset_calls == 2
+
+
+def test_resize_redraw_failure_quits_full_screen() -> None:
+    class FullScreenOutput(DummyOutput):
+        def __init__(self) -> None:
+            self.alternate_screen_entered = 0
+            self.alternate_screen_quit = 0
+
+        def enter_alternate_screen(self) -> None:
+            self.alternate_screen_entered += 1
+
+        def quit_alternate_screen(self) -> None:
+            self.alternate_screen_quit += 1
+
+    output = FullScreenOutput()
+    redraw_error = RuntimeError("redraw failed")
+    render_count = 0
+
+    def before_render(app: Application[None]) -> None:
+        nonlocal render_count
+        render_count += 1
+
+        if render_count == 2:
+            app.exit(exception=redraw_error)
+
+        if render_count >= 2:
+            raise redraw_error
+
+    with create_pipe_input() as input:
+        app: Application[None] = Application(
+            full_screen=True,
+            input=input,
+            output=output,
+            before_render=before_render,
+        )
+
+        def resize() -> None:
+            with pytest.raises(RuntimeError, match="redraw failed"):
+                app._on_resize()
+
+        with pytest.raises(RuntimeError, match="redraw failed"):
+            app.run(pre_run=lambda: asyncio.get_running_loop().call_soon(resize))
+
+    assert output.alternate_screen_entered == 1
+    assert output.alternate_screen_quit == 1