diff --git a/src/prompt_toolkit/application/run_in_terminal.py b/src/prompt_toolkit/application/run_in_terminal.py
index 24bae836b..110d89044 100644
--- a/src/prompt_toolkit/application/run_in_terminal.py
+++ b/src/prompt_toolkit/application/run_in_terminal.py
@@ -107,10 +107,22 @@ async def f():
     finally:
         # Redraw interface again.
         try:
-            app._running_in_terminal = False
-            app.renderer.reset()
-            app._request_absolute_cursor_position()
-            app._redraw()
+            try:
+                app.renderer.reset()
+                app._request_absolute_cursor_position()
+
+                # Wait for the CPR response before redrawing (rendering is
+                # still disabled). Otherwise, the first paint doesn't know how
+                # much space is available below the cursor and gets the
+                # layout's preferred height, right below the new output. Once
+                # the response arrives, the layout would be painted again,
+                # extended to the bottom of the terminal, which looks like a
+                # jump.
+                if app.output.responds_to_cpr:
+                    await app.renderer.wait_for_cpr_responses()
+            finally:
+                app._running_in_terminal = False
+                app._redraw()
         finally:
             # (Check for `.done()`, because it can be that this future was
             # cancelled.)
diff --git a/tests/test_run_in_terminal.py b/tests/test_run_in_terminal.py
new file mode 100644
index 000000000..9e3a7b5ca
--- /dev/null
+++ b/tests/test_run_in_terminal.py
@@ -0,0 +1,82 @@
+"""
+Test how `in_terminal` repaints the application afterwards.
+"""
+
+from __future__ import annotations
+
+import asyncio
+import io
+
+from prompt_toolkit.application import Application, in_terminal
+from prompt_toolkit.data_structures import Size
+from prompt_toolkit.input.defaults import create_pipe_input
+from prompt_toolkit.layout import FormattedTextControl, HSplit, Layout, Window
+from prompt_toolkit.output.vt100 import Vt100_Output
+
+
+class _TTY(io.StringIO):
+    "Emulate a terminal stdout, so that the output responds to CPR."
+
+    def isatty(self) -> bool:
+        return True
+
+
+def _run(send_cpr_response: bool) -> list[bool]:
+    """
+    Run an inline application, run `in_terminal` once it got its first CPR
+    response, and return for each paint after that (until exiting) whether
+    the renderer knew the space below the cursor.
+    """
+    heights_known: list[bool] = []
+
+    async def main() -> None:
+        with create_pipe_input() as inp:
+            app: Application[None] = Application(
+                layout=Layout(
+                    HSplit(
+                        [
+                            Window(FormattedTextControl("input"), height=1),
+                            Window(),
+                            Window(FormattedTextControl("toolbar"), height=1),
+                        ]
+                    )
+                ),
+                input=inp,
+                output=Vt100_Output(_TTY(), lambda: Size(rows=24, columns=80)),
+            )
+
+            async def suspend() -> None:
+                # Answer the CPR request done when the application started.
+                inp.send_text("\x1b[1;1R")
+                await app.renderer.wait_for_cpr_responses()
+
+                def after_render(_: object) -> None:
+                    if not app.is_done:
+                        heights_known.append(app.renderer.height_is_known)
+
+                async with in_terminal():
+                    app.after_render += after_render
+                    if send_cpr_response:
+                        # Input is detached here. This is read once it gets
+                        # attached again, after `in_terminal` requests the
+                        # cursor position.
+                        inp.send_text("\x1b[5;1R")
+
+                app.exit()
+
+            app.pre_run_callables.append(lambda: app.create_background_task(suspend()))
+            await app.run_async()
+
+    asyncio.run(main())
+    return heights_known
+
+
+def test_in_terminal_repaints_after_cpr_response():
+    # Paint once, knowing the available height, so that the layout doesn't
+    # jump.
+    assert _run(send_cpr_response=True) == [True]
+
+
+def test_in_terminal_repaints_without_cpr_response():
+    # When the response doesn't arrive, still repaint after the timeout.
+    assert _run(send_cpr_response=False) == [False]