diff --git a/mkdocs/commands/build.py b/mkdocs/commands/build.py
index 3a09a014..7d339909 100644
--- a/mkdocs/commands/build.py
+++ b/mkdocs/commands/build.py
@@ -131,8 +131,7 @@ def _build_extra_template(template_name: str, files: Files, config: MkDocsConfig
         return
 
     try:
-        with open(file.abs_src_path, encoding='utf-8', errors='strict') as f:
-            template = jinja2.Template(f.read())
+        template = jinja2.Template(file.content_string)
     except Exception as e:
         log.warning(f"Error reading template '{template_name}': {e}")
         return
diff --git a/mkdocs/plugins.py b/mkdocs/plugins.py
index aaf3b203..f38bbe7f 100644
--- a/mkdocs/plugins.py
+++ b/mkdocs/plugins.py
@@ -323,6 +323,8 @@ class BasePlugin(Generic[SomeConfig]):
 
     def on_page_read_source(self, /, *, page: Page, config: MkDocsConfig) -> str | None:
         """
+        Deprecated: Since MkDocs 1.6, instead set `content_bytes`/`content_string` of a `File`.
+
         The `on_page_read_source` event can replace the default mechanism to read
         the contents of a page's source from the filesystem.
 
diff --git a/mkdocs/structure/files.py b/mkdocs/structure/files.py
index c200ff82..5dae027b 100644
--- a/mkdocs/structure/files.py
+++ b/mkdocs/structure/files.py
@@ -170,28 +170,52 @@ class File:
     """
     A MkDocs File object.
 
-    Points to the source and destination locations of a file.
+    It represents how the contents of one file should be populated in the destination site.
 
-    The `path` argument must be a path that exists relative to `src_dir`.
+    A file always has its `abs_dest_path` (obtained by joining `dest_dir` and `dest_path`),
+    where the `dest_dir` is understood to be the *site* directory.
 
-    The `src_dir` and `dest_dir` must be absolute paths on the local file system.
+    `content_bytes`/`content_string` (new in MkDocs 1.6) can always be used to obtain the file's
+    content. But it may be backed by one of the two sources:
 
-    The `use_directory_urls` argument controls how destination paths are generated. If `False`, a Markdown file is
-    mapped to an HTML file of the same name (the file extension is changed to `.html`). If True, a Markdown file is
-    mapped to an HTML index file (`index.html`) nested in a directory using the "name" of the file in `path`. The
-    `use_directory_urls` argument has no effect on non-Markdown files.
+    *   A physical source file at `abs_src_path` (by default obtained by joining `src_dir` and
+        `src_uri`). `src_dir` is understood to be the *docs* directory.
 
-    File objects have the following properties, which are Unicode strings:
+        Then `content_bytes`/`content_string` will read the file at `abs_src_path`.
+
+        `src_dir` *should* be populated for real files and should be `None` for generated files.
+
+    *   Since MkDocs 1.6 a file may alternatively be stored in memory - `content_string`/`content_bytes`.
+
+        Then `src_dir` and `abs_src_path` will remain `None`. `content_bytes`/`content_string` need
+        to be written to, or populated through the `content` argument in the constructor.
+
+        But `src_uri` is still populated for such files as well! The virtual file pretends as if it
+        originated from that path in the `docs` directory, and other values are derived.
+
+    For static files the file is just copied to the destination, and `dest_uri` equals `src_uri`.
+
+    For Markdown files (determined by the file extension in `src_uri`) the destination content
+    will be the rendered content, and `dest_uri` will have the `.html` extension and some
+    additional transformations to the path, based on `use_directory_urls`.
     """
 
     src_uri: str
     """The pure path (always '/'-separated) of the source file relative to the source directory."""
 
     use_directory_urls: bool
-    """Whether directory URLs ('foo/') should be used or not ('foo.html')."""
+    """Whether directory URLs ('foo/') should be used or not ('foo.html').
 
-    src_dir: str
-    """The OS path of the source directory (top-level docs_dir) that the source file originates from."""
+    If `False`, a Markdown file is mapped to an HTML file of the same name (the file extension is
+    changed to `.html`). If True, a Markdown file is mapped to an HTML index file (`index.html`)
+    nested in a directory using the "name" of the file in `path`. Non-Markdown files retain their
+    original path.
+    """
+
+    src_dir: str | None
+    """The OS path of the top-level directory that the source file originates from.
+
+    Assumed to be the *docs_dir*; not populated for generated files."""
 
     dest_dir: str
     """The OS path of the destination directory (top-level site_dir) that the file should be copied to."""
@@ -202,6 +226,12 @@ class File:
     generated_by: str | None = None
     """If not None, indicates that a plugin generated this file on the fly."""
 
+    _content: str | bytes | None = None
+    """If set, the file's content will be read from here.
+
+    This logic is handled by `content_bytes`/`content_string`, which should be used instead of
+    accessing this attribute."""
+
     @property
     def src_path(self) -> str:
         """Same as `src_uri` (and synchronized with it) but will use backslashes on Windows. Discouraged."""
@@ -225,7 +255,7 @@ class File:
     def __init__(
         self,
         path: str,
-        src_dir: str,
+        src_dir: str | None,
         dest_dir: str,
         use_directory_urls: bool,
         *,
@@ -292,8 +322,14 @@ class File:
     """The URI of the destination file relative to the destination directory as a string."""
 
     @cached_property
-    def abs_src_path(self) -> str:
-        """The absolute concrete path of the source file. Will use backslashes on Windows."""
+    def abs_src_path(self) -> str | None:
+        """
+        The absolute concrete path of the source file. Will use backslashes on Windows.
+
+        Note: do not use this path to read the file, prefer `content_bytes`/`content_string`.
+        """
+        if self.src_dir is None:
+            return None
         return os.path.normpath(os.path.join(self.src_dir, self.src_uri))
 
     @cached_property
@@ -305,18 +341,80 @@ class File:
         """Return url for file relative to other file."""
         return utils.get_relative_url(self.url, other.url if isinstance(other, File) else other)
 
+    @property
+    def content_bytes(self) -> bytes:
+        """
+        Get the content of this file as a bytestring.
+
+        May raise if backed by a real file (`abs_src_path`) if it cannot be read.
+
+        If used as a setter, it defines the content of the file, and `abs_src_path` becomes unset.
+        """
+        content = self._content
+        if content is None:
+            assert self.abs_src_path is not None
+            with open(self.abs_src_path, 'rb') as f:
+                return f.read()
+        if not isinstance(content, bytes):
+            content = content.encode()
+        return content
+
+    @content_bytes.setter
+    def content_bytes(self, value: bytes):
+        assert isinstance(value, bytes)
+        self._content = value
+        self.abs_src_path = None
+
+    @property
+    def content_string(self) -> str:
+        """
+        Get the content of this file as a string. Assumes UTF-8 encoding, may raise.
+
+        May also raise if backed by a real file (`abs_src_path`) if it cannot be read.
+
+        If used as a setter, it defines the content of the file, and `abs_src_path` becomes unset.
+        """
+        content = self._content
+        if content is None:
+            assert self.abs_src_path is not None
+            with open(self.abs_src_path, encoding='utf-8-sig', errors='strict') as f:
+                return f.read()
+        if not isinstance(content, str):
+            content = content.decode('utf-8-sig', errors='strict')
+        return content
+
+    @content_string.setter
+    def content_string(self, value: str):
+        assert isinstance(value, str)
+        self._content = value
+        self.abs_src_path = None
+
     def copy_file(self, dirty: bool = False) -> None:
         """Copy source file to destination, ensuring parent directories exist."""
         if dirty and not self.is_modified():
             log.debug(f"Skip copying unmodified file: '{self.src_uri}'")
-        else:
-            log.debug(f"Copying media file: '{self.src_uri}'")
+            return
+        log.debug(f"Copying media file: '{self.src_uri}'")
+        output_path = self.abs_dest_path
+        os.makedirs(os.path.dirname(output_path), exist_ok=True)
+        content = self._content
+        if content is None:
+            assert self.abs_src_path is not None
             try:
-                utils.copy_file(self.abs_src_path, self.abs_dest_path)
+                utils.copy_file(self.abs_src_path, output_path)
             except shutil.SameFileError:
                 pass  # Let plugins write directly into site_dir.
+        elif isinstance(content, str):
+            with open(output_path, 'w', encoding='utf-8') as output_file:
+                output_file.write(content)
+        else:
+            with open(output_path, 'wb') as output_file:
+                output_file.write(content)
 
     def is_modified(self) -> bool:
+        if self._content is not None:
+            return True
+        assert self.abs_src_path is not None
         if os.path.isfile(self.abs_dest_path):
             return os.path.getmtime(self.abs_dest_path) < os.path.getmtime(self.abs_src_path)
         return True
diff --git a/mkdocs/structure/pages.py b/mkdocs/structure/pages.py
index 3e892b17..b7e949cb 100644
--- a/mkdocs/structure/pages.py
+++ b/mkdocs/structure/pages.py
@@ -208,8 +208,7 @@ class Page(StructureItem):
         source = config.plugins.on_page_read_source(page=self, config=config)
         if source is None:
             try:
-                with open(self.file.abs_src_path, encoding='utf-8-sig', errors='strict') as f:
-                    source = f.read()
+                source = self.file.content_string
             except OSError:
                 log.error(f'File not found: {self.file.src_path}')
                 raise
diff --git a/mkdocs/tests/build_tests.py b/mkdocs/tests/build_tests.py
index 9e9d6c0a..2ad93532 100644
--- a/mkdocs/tests/build_tests.py
+++ b/mkdocs/tests/build_tests.py
@@ -274,14 +274,14 @@ class BuildTests(PathAssertionMixin, unittest.TestCase):
     # Test build._build_extra_template
 
     @tempdir()
-    @mock.patch('mkdocs.commands.build.open', mock.mock_open(read_data='template content'))
+    @mock.patch('mkdocs.structure.files.open', mock.mock_open(read_data='template content'))
     def test_build_extra_template(self, site_dir):
         cfg = load_config(site_dir=site_dir)
         fs = [File('foo.html', cfg.docs_dir, cfg.site_dir, cfg.use_directory_urls)]
         files = Files(fs)
         build._build_extra_template('foo.html', files, cfg, mock.Mock())
 
-    @mock.patch('mkdocs.commands.build.open', mock.mock_open(read_data='template content'))
+    @mock.patch('mkdocs.structure.files.open', mock.mock_open(read_data='template content'))
     def test_skip_missing_extra_template(self):
         cfg = load_config()
         fs = [File('foo.html', cfg.docs_dir, cfg.site_dir, cfg.use_directory_urls)]
@@ -293,7 +293,7 @@ class BuildTests(PathAssertionMixin, unittest.TestCase):
             "WARNING:mkdocs.commands.build:Template skipped: 'missing.html' not found in docs_dir.",
         )
 
-    @mock.patch('mkdocs.commands.build.open', mock.Mock(side_effect=OSError('Error message.')))
+    @mock.patch('mkdocs.structure.files.open', mock.Mock(side_effect=OSError('Error message.')))
     def test_skip_ioerror_extra_template(self):
         cfg = load_config()
         fs = [File('foo.html', cfg.docs_dir, cfg.site_dir, cfg.use_directory_urls)]
@@ -305,7 +305,7 @@ class BuildTests(PathAssertionMixin, unittest.TestCase):
             "WARNING:mkdocs.commands.build:Error reading template 'foo.html': Error message.",
         )
 
-    @mock.patch('mkdocs.commands.build.open', mock.mock_open(read_data=''))
+    @mock.patch('mkdocs.structure.files.open', mock.mock_open(read_data=''))
     def test_skip_extra_template_empty_output(self):
         cfg = load_config()
         fs = [File('foo.html', cfg.docs_dir, cfg.site_dir, cfg.use_directory_urls)]
@@ -350,7 +350,7 @@ class BuildTests(PathAssertionMixin, unittest.TestCase):
         self.assertEqual(page.content, None)
 
     @tempdir(files={'index.md': 'new page content'})
-    @mock.patch('mkdocs.structure.pages.open', side_effect=OSError('Error message.'))
+    @mock.patch('mkdocs.structure.files.open', side_effect=OSError('Error message.'))
     def test_populate_page_read_error(self, docs_dir, mock_open):
         cfg = load_config(docs_dir=docs_dir)
         file = File('missing.md', cfg.docs_dir, cfg.site_dir, cfg.use_directory_urls)
@@ -763,7 +763,7 @@ class BuildTests(PathAssertionMixin, unittest.TestCase):
             # Plugin 2 reads that file and uses it to configure the nav.
             f = files.get_file_from_path('SUMMARY.md')
             assert f is not None
-            config.nav = Path(f.abs_src_path).read_text().splitlines()
+            config.nav = f.content_string.splitlines()
 
         for serve_url in None, 'http://localhost:123/':
             for exclude in 'full', 'drafts', 'nav', None:
diff --git a/mkdocs/tests/structure/file_tests.py b/mkdocs/tests/structure/file_tests.py
index dec70449..36703176 100644
--- a/mkdocs/tests/structure/file_tests.py
+++ b/mkdocs/tests/structure/file_tests.py
@@ -275,6 +275,24 @@ class TestFiles(PathAssertionMixin, unittest.TestCase):
         del f.name
         self.assertFalse(f.is_documentation_page())
 
+    def test_generated_file(self):
+        f = File(
+            'foo/bar.md',
+            src_dir=None,
+            dest_dir='/path/to/site',
+            use_directory_urls=False,
+        )
+        f.content_string = 'вміст'
+        f.generated_by = 'some-plugin'
+        self.assertEqual(f.generated_by, 'some-plugin')
+        self.assertEqual(f.src_uri, 'foo/bar.md')
+        self.assertIsNone(f.abs_src_path)
+        self.assertIsNone(f.src_dir)
+        self.assertEqual(f.dest_uri, 'foo/bar.html')
+        self.assertPathsEqual(f.abs_dest_path, '/path/to/site/foo/bar.html')
+        self.assertEqual(f.content_string, 'вміст')
+        self.assertEqual(f.edit_uri, None)
+
     def test_files(self):
         fs = [
             File('index.md', '/path/to/docs', '/path/to/site', use_directory_urls=True),
@@ -610,6 +628,8 @@ class TestFiles(PathAssertionMixin, unittest.TestCase):
     @tempdir(files={'test.txt': 'source content'})
     def test_copy_file_clean_modified(self, src_dir, dest_dir):
         file = File('test.txt', src_dir, dest_dir, use_directory_urls=False)
+        self.assertEqual(file.content_string, 'source content')
+        self.assertEqual(file.content_bytes, b'source content')
         file.is_modified = mock.Mock(return_value=True)
         dest_path = os.path.join(dest_dir, 'test.txt')
         file.copy_file(dirty=False)
@@ -639,6 +659,28 @@ class TestFiles(PathAssertionMixin, unittest.TestCase):
         with open(dest_path, encoding='utf-8') as f:
             self.assertEqual(f.read(), 'destination content')
 
+    @tempdir()
+    def test_copy_file_from_content(self, dest_dir):
+        file = File('test.txt', src_dir='unused', dest_dir=dest_dir, use_directory_urls=False)
+        file.content_string = 'ö'
+        self.assertIsNone(file.abs_src_path)
+        dest_path = os.path.join(dest_dir, 'test.txt')
+
+        file.copy_file()
+        self.assertPathIsFile(dest_path)
+        with open(dest_path, encoding='utf-8') as f:
+            self.assertEqual(f.read(), 'ö')
+
+        file.content_bytes = b'\x01\x02\x03'
+        file.copy_file()
+        with open(dest_path, 'rb') as f:
+            self.assertEqual(f.read(), b'\x01\x02\x03')
+
+        file.content_bytes = b'\xc3\xb6'
+        file.copy_file()
+        with open(dest_path, encoding='utf-8') as f:
+            self.assertEqual(f.read(), 'ö')
+
     def test_files_append_remove_src_paths(self):
         fs = [
             File('index.md', '/path/to/docs', '/path/to/site', use_directory_urls=True),
diff --git a/mkdocs/tests/structure/page_tests.py b/mkdocs/tests/structure/page_tests.py
index 094a2c60..ee6aa159 100644
--- a/mkdocs/tests/structure/page_tests.py
+++ b/mkdocs/tests/structure/page_tests.py
@@ -757,7 +757,7 @@ class RelativePathExtensionTests(unittest.TestCase):
         fs = [File(f, cfg.docs_dir, cfg.site_dir, cfg.use_directory_urls) for f in files]
         pg = Page('Foo', fs[0], cfg)
 
-        with mock.patch('mkdocs.structure.pages.open', mock.mock_open(read_data=content)):
+        with mock.patch('mkdocs.structure.files.open', mock.mock_open(read_data=content)):
             pg.read_source(cfg)
         if logs:
             with self.assertLogs('mkdocs.structure.pages') as cm: