diff --git a/src/prompt_toolkit/input/ansi_escape_sequences.py b/src/prompt_toolkit/input/ansi_escape_sequences.py
index 1fba418b7..bb73b5e84 100644
--- a/src/prompt_toolkit/input/ansi_escape_sequences.py
+++ b/src/prompt_toolkit/input/ansi_escape_sequences.py
@@ -77,6 +77,8 @@
     "\x1b[Z": Keys.BackTab,  # shift + tab
     "\x1b\x09": Keys.BackTab,  # Linux console
     "\x1b[~": Keys.BackTab,  # Windows console
+    "\x1b[I": Keys.FocusIn,
+    "\x1b[O": Keys.FocusOut,
     # --
     # Function keys.
     "\x1bOP": Keys.F1,
diff --git a/src/prompt_toolkit/key_binding/bindings/focus.py b/src/prompt_toolkit/key_binding/bindings/focus.py
index 24aa3ce39..12baf7bac 100644
--- a/src/prompt_toolkit/key_binding/bindings/focus.py
+++ b/src/prompt_toolkit/key_binding/bindings/focus.py
@@ -1,10 +1,13 @@
 from __future__ import annotations
 
+from prompt_toolkit.key_binding.key_bindings import KeyBindings
 from prompt_toolkit.key_binding.key_processor import KeyPressEvent
+from prompt_toolkit.keys import Keys
 
 __all__ = [
     "focus_next",
     "focus_previous",
+    "load_focus_bindings",
 ]
 
 E = KeyPressEvent
@@ -24,3 +27,20 @@ def focus_previous(event: E) -> None:
     (Often bound to the `BackTab` key.)
     """
     event.app.layout.focus_previous()
+
+
+def load_focus_bindings() -> KeyBindings:
+    """Key bindings for terminal focus events."""
+    key_bindings = KeyBindings()
+
+    @key_bindings.add(Keys.FocusIn, save_before=lambda e: False)
+    def _(event: E) -> None:
+        """Redraw the application after the terminal restores its screen."""
+        event.app.renderer.erase(leave_alternate_screen=False)
+        event.app.invalidate()
+
+    @key_bindings.add(Keys.FocusOut, save_before=lambda e: False)
+    def _(event: E) -> None:
+        """Consume the focus-out event."""
+
+    return key_bindings
diff --git a/src/prompt_toolkit/key_binding/defaults.py b/src/prompt_toolkit/key_binding/defaults.py
index 6c2657116..3b8c4ad3e 100644
--- a/src/prompt_toolkit/key_binding/defaults.py
+++ b/src/prompt_toolkit/key_binding/defaults.py
@@ -15,6 +15,7 @@
     load_emacs_search_bindings,
     load_emacs_shift_selection_bindings,
 )
+from prompt_toolkit.key_binding.bindings.focus import load_focus_bindings
 from prompt_toolkit.key_binding.bindings.mouse import load_mouse_bindings
 from prompt_toolkit.key_binding.bindings.vi import (
     load_vi_bindings,
@@ -59,5 +60,6 @@ def load_key_bindings() -> KeyBindingsBase:
             # Active, even when no buffer has been focused.
             load_mouse_bindings(),
             load_cpr_bindings(),
+            load_focus_bindings(),
         ]
     )
diff --git a/src/prompt_toolkit/keys.py b/src/prompt_toolkit/keys.py
index ee52aee86..b526732bc 100644
--- a/src/prompt_toolkit/keys.py
+++ b/src/prompt_toolkit/keys.py
@@ -182,6 +182,8 @@ class Keys(str, Enum):
 
     CPRResponse = "<cursor-position-response>"
     Vt100MouseEvent = "<vt100-mouse-event>"
+    FocusIn = "<focus-in>"
+    FocusOut = "<focus-out>"
     WindowsMouseEvent = "<windows-mouse-event>"
     BracketedPaste = "<bracketed-paste>"
 
diff --git a/src/prompt_toolkit/output/base.py b/src/prompt_toolkit/output/base.py
index 6ba09fdd0..da6f5790c 100644
--- a/src/prompt_toolkit/output/base.py
+++ b/src/prompt_toolkit/output/base.py
@@ -187,6 +187,17 @@ def enable_bracketed_paste(self) -> None:
     def disable_bracketed_paste(self) -> None:
         "For vt100 only."
 
+    @property
+    def supports_focus_reporting(self) -> bool:
+        "True if this output can receive terminal focus events."
+        return False
+
+    def enable_focus_reporting(self) -> None:
+        "For vt100 only."
+
+    def disable_focus_reporting(self) -> None:
+        "For vt100 only."
+
     def reset_cursor_key_mode(self) -> None:
         """
         For vt100 only.
diff --git a/src/prompt_toolkit/output/conemu.py b/src/prompt_toolkit/output/conemu.py
index 636994494..e24175681 100644
--- a/src/prompt_toolkit/output/conemu.py
+++ b/src/prompt_toolkit/output/conemu.py
@@ -56,6 +56,9 @@ def __getattr__(self, name: str) -> Any:
             "get_win32_screen_buffer_info",
             "enable_bracketed_paste",
             "disable_bracketed_paste",
+            "supports_focus_reporting",
+            "enable_focus_reporting",
+            "disable_focus_reporting",
         ):
             return getattr(self.win32_output, name)
         else:
diff --git a/src/prompt_toolkit/output/vt100.py b/src/prompt_toolkit/output/vt100.py
index b2712254f..cf94a8f0e 100644
--- a/src/prompt_toolkit/output/vt100.py
+++ b/src/prompt_toolkit/output/vt100.py
@@ -611,6 +611,22 @@ def enable_bracketed_paste(self) -> None:
     def disable_bracketed_paste(self) -> None:
         self.write_raw("\x1b[?2004l")
 
+    @property
+    def supports_focus_reporting(self) -> bool:
+        if is_dumb_terminal(self.term):
+            return False
+
+        try:
+            return self.stdout.isatty()
+        except ValueError:
+            return False
+
+    def enable_focus_reporting(self) -> None:
+        self.write_raw("\x1b[?1004h")
+
+    def disable_focus_reporting(self) -> None:
+        self.write_raw("\x1b[?1004l")
+
     def reset_cursor_key_mode(self) -> None:
         """
         For vt100 only.
diff --git a/src/prompt_toolkit/output/windows10.py b/src/prompt_toolkit/output/windows10.py
index 2b7e596e4..784f3621f 100644
--- a/src/prompt_toolkit/output/windows10.py
+++ b/src/prompt_toolkit/output/windows10.py
@@ -76,6 +76,9 @@ def __getattr__(self, name: str) -> Any:
             "get_rows_below_cursor_position",
             "scroll_buffer_to_prompt",
             "get_win32_screen_buffer_info",
+            "supports_focus_reporting",
+            "enable_focus_reporting",
+            "disable_focus_reporting",
             # "enable_mouse_support",
             # "disable_mouse_support",
             # "enable_bracketed_paste",
diff --git a/src/prompt_toolkit/renderer.py b/src/prompt_toolkit/renderer.py
index fcfde223e..7be245ee2 100644
--- a/src/prompt_toolkit/renderer.py
+++ b/src/prompt_toolkit/renderer.py
@@ -362,6 +362,7 @@ def __init__(
         self._in_alternate_screen = False
         self._mouse_support_enabled = False
         self._bracketed_paste_enabled = False
+        self._focus_reporting_enabled = False
         self._cursor_key_mode_reset = False
 
         # Future set when we are waiting for a CPR flag.
@@ -421,6 +422,10 @@ def reset(self, _scroll: bool = False, leave_alternate_screen: bool = True) -> N
             self.output.disable_bracketed_paste()
             self._bracketed_paste_enabled = False
 
+        if self._focus_reporting_enabled:
+            self.output.disable_focus_reporting()
+            self._focus_reporting_enabled = False
+
         self.output.reset_cursor_shape()
         self.output.show_cursor()
 
@@ -609,6 +614,11 @@ def render(
             self.output.enable_bracketed_paste()
             self._bracketed_paste_enabled = True
 
+        # Enable focus event reporting on terminals that support it.
+        if not self._focus_reporting_enabled and output.supports_focus_reporting:
+            output.enable_focus_reporting()
+            self._focus_reporting_enabled = True
+
         # Reset cursor key mode.
         if not self._cursor_key_mode_reset:
             self.output.reset_cursor_key_mode()
diff --git a/tests/test_focus_bindings.py b/tests/test_focus_bindings.py
new file mode 100644
index 000000000..434bb56eb
--- /dev/null
+++ b/tests/test_focus_bindings.py
@@ -0,0 +1,101 @@
+from __future__ import annotations
+
+from contextlib import contextmanager
+
+from prompt_toolkit.application import Application
+from prompt_toolkit.application.current import set_app
+from prompt_toolkit.data_structures import Point
+from prompt_toolkit.input.defaults import create_pipe_input
+from prompt_toolkit.key_binding.key_processor import KeyPress
+from prompt_toolkit.keys import Keys
+from prompt_toolkit.layout import Layout, Window
+from prompt_toolkit.layout.screen import Screen
+from prompt_toolkit.output import DummyOutput
+
+
+class _RecordingOutput(DummyOutput):
+    def __init__(self) -> None:
+        self.calls: list[tuple[str, tuple[int, ...]]] = []
+
+    @property
+    def supports_focus_reporting(self) -> bool:
+        return True
+
+    def enable_focus_reporting(self) -> None:
+        self.calls.append(("enable_focus_reporting", ()))
+
+    def disable_focus_reporting(self) -> None:
+        self.calls.append(("disable_focus_reporting", ()))
+
+    def cursor_backward(self, amount: int) -> None:
+        self.calls.append(("cursor_backward", (amount,)))
+
+    def cursor_up(self, amount: int) -> None:
+        self.calls.append(("cursor_up", (amount,)))
+
+    def erase_down(self) -> None:
+        self.calls.append(("erase_down", ()))
+
+
+@contextmanager
+def _create_app(output: DummyOutput):
+    with create_pipe_input() as pipe_input:
+        app = Application(
+            layout=Layout(Window()),
+            input=pipe_input,
+            output=output,
+        )
+
+        def create_background_task(coroutine, **kwargs):
+            coroutine.close()
+            return None
+
+        app.create_background_task = create_background_task
+
+        with set_app(app):
+            yield app
+
+
+def test_focus_in_erases_and_invalidates_screen():
+    output = _RecordingOutput()
+
+    with _create_app(output) as app:
+        invalidated = False
+
+        def invalidate() -> None:
+            nonlocal invalidated
+            invalidated = True
+
+        app.invalidate = invalidate
+        app.renderer._last_screen = Screen()
+        app.renderer._in_alternate_screen = True
+        app.renderer._cursor_pos = Point(x=7, y=2)
+        output.calls.clear()
+
+        app.key_processor.feed(KeyPress(Keys.FocusIn, "\x1b[I"))
+        app.key_processor.process_keys()
+
+        assert app.renderer._last_screen is None
+        assert app.renderer._in_alternate_screen
+        assert invalidated
+        assert output.calls == [
+            ("cursor_backward", (7,)),
+            ("cursor_up", (2,)),
+            ("erase_down", ()),
+        ]
+
+
+def test_renderer_enables_and_disables_focus_reporting():
+    output = _RecordingOutput()
+
+    with _create_app(output) as app:
+        app.renderer.render(app, app.layout)
+        app.renderer.render(app, app.layout)
+
+        focus_calls = [name for name, _ in output.calls if "focus_reporting" in name]
+        assert focus_calls == ["enable_focus_reporting"]
+
+        app.renderer.reset()
+
+        focus_calls = [name for name, _ in output.calls if "focus_reporting" in name]
+        assert focus_calls == ["enable_focus_reporting", "disable_focus_reporting"]
diff --git a/tests/test_inputstream.py b/tests/test_inputstream.py
index ab1b03689..7588ee476 100644
--- a/tests/test_inputstream.py
+++ b/tests/test_inputstream.py
@@ -139,3 +139,10 @@ def test_cpr_response_2(processor, stream):
     assert len(processor.keys) == 2
     assert processor.keys[0].key == Keys.CPRResponse
     assert processor.keys[1].key == Keys.ControlJ
+
+
+def test_focus_events(processor, stream):
+    stream.feed("\x1b[I\x1b[O")
+
+    assert [key.key for key in processor.keys] == [Keys.FocusIn, Keys.FocusOut]
+    assert [key.data for key in processor.keys] == ["\x1b[I", "\x1b[O"]
diff --git a/tests/test_vt100_output.py b/tests/test_vt100_output.py
index ca62be54e..01fa5d0fe 100644
--- a/tests/test_vt100_output.py
+++ b/tests/test_vt100_output.py
@@ -1,6 +1,18 @@
 from __future__ import annotations
 
-from prompt_toolkit.output.vt100 import _256_colors, _get_closest_ansi_color
+from io import StringIO
+
+from prompt_toolkit.data_structures import Size
+from prompt_toolkit.output.vt100 import (
+    Vt100_Output,
+    _256_colors,
+    _get_closest_ansi_color,
+)
+
+
+class _TTYStringIO(StringIO):
+    def isatty(self) -> bool:
+        return True
 
 
 def test_get_closest_ansi_color():
@@ -29,3 +41,17 @@ def test_256_colors():
     # Grayscale
     assert _256_colors[(8, 8, 8)] == 232  # First grayscale level
     assert _256_colors[(238, 238, 238)] == 255  # Last grayscale level
+
+
+def test_focus_reporting():
+    stdout = _TTYStringIO()
+    output = Vt100_Output(stdout, lambda: Size(rows=24, columns=80), term="xterm")
+
+    assert output.supports_focus_reporting
+
+    output.enable_focus_reporting()
+    output.flush()
+    output.disable_focus_reporting()
+    output.flush()
+
+    assert stdout.getvalue() == "\x1b[?1004h\x1b[?1004l"