diff --git a/qutebrowser/mainwindow/prompt.py b/qutebrowser/mainwindow/prompt.py
index c8045c0e8..7c4124da0 100644
--- a/qutebrowser/mainwindow/prompt.py
+++ b/qutebrowser/mainwindow/prompt.py
@@ -665,6 +665,8 @@ class FilenamePrompt(_BasePrompt):
         self._init_texts(question)
         self._init_key_label()
 
+        self._user_expanded = False
+
         self._lineedit = LineEdit(self)
         if question.default:
             self._lineedit.setText(question.default)
@@ -698,6 +700,11 @@ class FilenamePrompt(_BasePrompt):
         if os.altsep is not None:
             separators += os.altsep
 
+        # If the path is not the same as the path with expanduser set a boolean
+        if os.path.expanduser(path) != path:
+            path = os.path.expanduser(path)
+            self._user_expanded = True
+
         dirname = os.path.dirname(path)
         basename = os.path.basename(path)
         if not tabbed:
@@ -746,6 +753,9 @@ class FilenamePrompt(_BasePrompt):
             # On Windows, when we have C:\foo and tab over .., we get C:\
             path = path.rstrip(os.sep)
 
+        if self._user_expanded:
+            path = path.replace(os.path.expanduser('~'), '~', 1)
+
         log.prompt.debug('Inserting path {}'.format(path))
         self._lineedit.setText(path)
         self._lineedit.setFocus()
diff --git a/tests/unit/mainwindow/test_prompt.py b/tests/unit/mainwindow/test_prompt.py
index 67403101c..352c6fc44 100644
--- a/tests/unit/mainwindow/test_prompt.py
+++ b/tests/unit/mainwindow/test_prompt.py
@@ -3,6 +3,7 @@
 # SPDX-License-Identifier: GPL-3.0-or-later
 
 import os
+import pathlib
 
 import pytest
 from qutebrowser.qt.core import Qt
@@ -113,3 +114,56 @@ class TestFileCompletion:
         """With / as path, show root contents."""
         prompt = get_prompt('/')
         assert prompt._file_model.rootPath() == '/'
+
+    @pytest.fixture
+    def home_path(self, monkeypatch, tmp_path):
+        homedir = str(tmp_path)
+        monkeypatch.setenv('HOME', homedir)  # POSIX
+        monkeypatch.setenv('USERPROFILE', homedir)  # Windows
+        assert str(pathlib.Path.home()) == homedir
+        return tmp_path
+
+    def test_expand_user(self, qtbot, get_prompt, home_path):
+        for directory in ['bar', 'bat', 'foo']:
+            (home_path / directory).mkdir()
+
+        prompt = get_prompt('/')
+        prompt._lineedit.setText('')
+        with qtbot.wait_signal(prompt._file_model.directoryLoaded):
+            # _set_fileview_root isn't run unless there is an actual keypress
+            qtbot.keyPress(prompt._lineedit, Qt.Key_AsciiTilde)
+
+            assert (pathlib.Path(prompt._file_model.rootPath()) /
+                    prompt._to_complete) == pathlib.Path.home()
+            # The first character on the lineedit should remain ~
+            prompt.item_focus('next')
+            prompt.item_focus('next')
+            assert prompt._lineedit.text()[0] == '~'
+
+    def test_expand_once(self, qtbot, get_prompt, home_path):
+        home_path.joinpath(*home_path.parts[1:]).mkdir(parents=True)
+
+        prompt = get_prompt('/')
+        prompt._lineedit.setText('~' + str(home_path))
+        with qtbot.wait_signal(prompt._file_model.directoryLoaded):
+            # _set_fileview_root isn't run unless there is an actual keypress
+            qtbot.keyPress(prompt._lineedit, Qt.Key_Slash)
+
+            # The second instance of home_path shouldn't be replaced with ~
+            assert prompt._lineedit.text()[:-1] == '~' + str(home_path)
+
+    def test_dont_contract(self, qtbot, get_prompt, home_path):
+        for directory in ['bar', 'bat', 'foo']:
+            (home_path / directory).mkdir()
+
+        prompt = get_prompt('/')
+        prompt._lineedit.setText(str(home_path))
+        with qtbot.wait_signal(prompt._file_model.directoryLoaded):
+            # _set_fileview_root isn't run unless there is an actual keypress
+            qtbot.keyPress(prompt._lineedit, Qt.Key_Slash)
+
+            prompt.item_focus('next')
+            prompt.item_focus('next')
+            # If $HOME is contracted to `~` this test will fail as that is unexpected
+            assert (prompt._lineedit.text() !=
+                    prompt._lineedit.text().replace(os.path.expanduser('~'), '~', 1))