diff --git a/telegram/_bot.py b/telegram/_bot.py
index 6cb51d2ae..5f4927cb8 100644
--- a/telegram/_bot.py
+++ b/telegram/_bot.py
@@ -1305,8 +1305,8 @@ class Bot(TelegramObject, AsyncContextManager["Bot"]):
 
         Args:
             chat_id (:obj:`int` | :obj:`str`): |chat_id_channel|
-            photo (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-                :class:`telegram.PhotoSize`): Photo to send.
+            photo (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` \
+                | :class:`pathlib.Path` | :class:`telegram.PhotoSize`): Photo to send.
                 |fileinput|
                 Lastly you can pass an existing :class:`telegram.PhotoSize` object to send.
 
@@ -1465,9 +1465,9 @@ class Bot(TelegramObject, AsyncContextManager["Bot"]):
 
         Args:
             chat_id (:obj:`int` | :obj:`str`): |chat_id_channel|
-            audio (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-                :class:`telegram.Audio`): Audio file to send.
-                |fileinput|
+            audio (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | \
+                :obj:`bytes` | :class:`pathlib.Path` | :class:`telegram.Audio`): Audio file to
+                send. |fileinput|
                 Lastly you can pass an existing :class:`telegram.Audio` object to send.
 
                 .. versionchanged:: 13.2
@@ -1617,8 +1617,8 @@ class Bot(TelegramObject, AsyncContextManager["Bot"]):
 
         Args:
             chat_id (:obj:`int` | :obj:`str`): |chat_id_channel|
-            document (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-                :class:`telegram.Document`): File to send.
+            document (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | \
+                :obj:`bytes` | :class:`pathlib.Path` | :class:`telegram.Document`): File to send.
                 |fileinput|
                 Lastly you can pass an existing :class:`telegram.Document` object to send.
 
@@ -1755,8 +1755,8 @@ class Bot(TelegramObject, AsyncContextManager["Bot"]):
 
         Args:
             chat_id (:obj:`int` | :obj:`str`): |chat_id_channel|
-            sticker (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-                :class:`telegram.Sticker`): Sticker to send.
+            sticker (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | \
+                :obj:`bytes` | :class:`pathlib.Path` | :class:`telegram.Sticker`): Sticker to send.
                 |fileinput| Video stickers can only be sent by a ``file_id``. Video and animated
                 stickers can't be sent via an HTTP URL.
 
@@ -1895,8 +1895,8 @@ class Bot(TelegramObject, AsyncContextManager["Bot"]):
 
         Args:
             chat_id (:obj:`int` | :obj:`str`): |chat_id_channel|
-            video (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-                :class:`telegram.Video`): Video file to send.
+            video (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` \
+                | :class:`pathlib.Path` | :class:`telegram.Video`): Video file to send.
                 |fileinput|
                 Lastly you can pass an existing :class:`telegram.Video` object to send.
 
@@ -2059,8 +2059,9 @@ class Bot(TelegramObject, AsyncContextManager["Bot"]):
 
         Args:
             chat_id (:obj:`int` | :obj:`str`): |chat_id_channel|
-            video_note (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-                :class:`telegram.VideoNote`): Video note to send.
+            video_note (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | \
+                :obj:`bytes` | :class:`pathlib.Path` | :class:`telegram.VideoNote`): Video note
+                to send.
                 Pass a file_id as String to send a video note that exists on the Telegram
                 servers (recommended) or upload a new video using multipart/form-data.
                 |uploadinput|
@@ -2209,9 +2210,9 @@ class Bot(TelegramObject, AsyncContextManager["Bot"]):
 
         Args:
             chat_id (:obj:`int` | :obj:`str`): |chat_id_channel|
-            animation (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-                :class:`telegram.Animation`): Animation to send.
-                |fileinput|
+            animation (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | \
+                :obj:`bytes` | :class:`pathlib.Path` | :class:`telegram.Animation`): Animation to
+                send. |fileinput|
                 Lastly you can pass an existing :class:`telegram.Animation` object to send.
 
                 .. versionchanged:: 13.2
@@ -2371,8 +2372,8 @@ class Bot(TelegramObject, AsyncContextManager["Bot"]):
 
         Args:
             chat_id (:obj:`int` | :obj:`str`): |chat_id_channel|
-            voice (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-                :class:`telegram.Voice`): Voice file to send.
+            voice (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` \
+                | :class:`pathlib.Path` | :class:`telegram.Voice`): Voice file to send.
                 |fileinput|
                 Lastly you can pass an existing :class:`telegram.Voice` object to send.
 
@@ -6370,8 +6371,9 @@ CUSTOM_EMOJI_IDENTIFIER_LIMIT` custom emoji identifiers can be specified.
 
         Args:
             user_id (:obj:`int`): User identifier of sticker file owner.
-            sticker (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path`):
-                A file with the sticker in the  ``".WEBP"``, ``".PNG"``, ``".TGS"`` or ``".WEBM"``
+            sticker (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | \
+                :obj:`bytes` | :class:`pathlib.Path`): A file with the sticker in the
+                ``".WEBP"``, ``".PNG"``, ``".TGS"`` or ``".WEBM"``
                 format. See `here <https://core.telegram.org/stickers>`_ for technical requirements
                 . |uploadinput|
 
@@ -6695,8 +6697,9 @@ CUSTOM_EMOJI_IDENTIFIER_LIMIT` custom emoji identifiers can be specified.
 
                 .. versionadded:: 21.1
 
-            thumbnail (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path`, \
-                optional): A **.WEBP** or **.PNG** image with the thumbnail, must
+            thumbnail (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | \
+                :obj:`bytes` | :class:`pathlib.Path`, optional): A **.WEBP** or **.PNG** image
+                with the thumbnail, must
                 be up to :tg-const:`telegram.constants.StickerSetLimit.MAX_STATIC_THUMBNAIL_SIZE`
                 kilobytes in size and have width and height of exactly
                 :tg-const:`telegram.constants.StickerSetLimit.STATIC_THUMB_DIMENSIONS` px, or a
diff --git a/telegram/_files/inputfile.py b/telegram/_files/inputfile.py
index 9a07f6d65..8f9c24a20 100644
--- a/telegram/_files/inputfile.py
+++ b/telegram/_files/inputfile.py
@@ -22,7 +22,7 @@ import mimetypes
 from typing import IO, Optional, Union
 from uuid import uuid4
 
-from telegram._utils.files import load_file
+from telegram._utils.files import guess_file_name, load_file
 from telegram._utils.strings import TextEncoding
 from telegram._utils.types import FieldTuple
 
@@ -53,9 +53,36 @@ class InputFile:
         attach (:obj:`bool`, optional): Pass :obj:`True` if the parameter this file belongs to in
             the request to Telegram should point to the multipart data via an ``attach://`` URI.
             Defaults to `False`.
+        read_file_handle (:obj:`bool`, optional): If :obj:`True` and :paramref:`obj` is a file
+            handle, the data will be read from the file handle on initialization of this object.
+            If :obj:`False`, the file handle will be passed on to the
+            `networking backend <telegram.request.BaseRequest.do_request>`_ which will have to
+            handle the reading. Defaults to :obj:`True`.
+
+            Tip:
+                If you upload extremely large files, you may want to set this to :obj:`False` to
+                avoid reading the complete file into memory. Additionally, this may be supported
+                better by the networking backend (in particular it is handled better by
+                the default :class:`~telegram.request.HTTPXRequest`).
+
+            Important:
+                If you set this to :obj:`False`, you have to ensure that the file handle is still
+                open when the request is made. In particular, the following snippet can *not* work
+                as expected.
+
+                .. code-block:: python
+
+                    with open('file.txt', 'rb') as file:
+                        input_file = InputFile(file, read_file_handle=False)
+
+                    # here the file handle is already closed and the upload will fail
+                    await bot.send_document(chat_id, input_file)
+
+            .. versionadded:: NEXT.VERSION
+
 
     Attributes:
-        input_file_content (:obj:`bytes`): The binary content of the file to send.
+        input_file_content (:obj:`bytes` | :class:`IO`): The binary content of the file to send.
         attach_name (:obj:`str`): Optional. If present, the parameter this file belongs to in
             the request to Telegram should point to the multipart data via a an URI of the form
             ``attach://<attach_name>`` URI.
@@ -71,14 +98,18 @@ class InputFile:
         obj: Union[IO[bytes], bytes, str],
         filename: Optional[str] = None,
         attach: bool = False,
+        read_file_handle: bool = True,
     ):
         if isinstance(obj, bytes):
-            self.input_file_content: bytes = obj
+            self.input_file_content: Union[bytes, IO[bytes]] = obj
         elif isinstance(obj, str):
             self.input_file_content = obj.encode(TextEncoding.UTF_8)
-        else:
+        elif read_file_handle:
             reported_filename, self.input_file_content = load_file(obj)
             filename = filename or reported_filename
+        else:
+            self.input_file_content = obj
+            filename = filename or guess_file_name(obj)
 
         self.attach_name: Optional[str] = "attached" + uuid4().hex if attach else None
 
@@ -95,8 +126,11 @@ class InputFile:
     def field_tuple(self) -> FieldTuple:
         """Field tuple representing the contents of the file for upload to the Telegram servers.
 
+        .. versionchanged:: NEXT.VERSION
+            Content may now be a file handle.
+
         Returns:
-            Tuple[:obj:`str`, :obj:`bytes`, :obj:`str`]:
+            Tuple[:obj:`str`, :obj:`bytes` | :class:`IO`, :obj:`str`]:
         """
         return self.filename, self.input_file_content, self.mimetype
 
diff --git a/telegram/_files/inputmedia.py b/telegram/_files/inputmedia.py
index 692369130..c33a87a2d 100644
--- a/telegram/_files/inputmedia.py
+++ b/telegram/_files/inputmedia.py
@@ -50,8 +50,8 @@ class InputMedia(TelegramObject):
 
     Args:
         media_type (:obj:`str`): Type of media that the instance represents.
-        media (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-            :class:`telegram.Animation` |  :class:`telegram.Audio` | \
+        media (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` | \
+            :class:`pathlib.Path` | :class:`telegram.Animation` |  :class:`telegram.Audio` | \
             :class:`telegram.Document` | :class:`telegram.PhotoSize` | \
             :class:`telegram.Video`): File to send.
             |fileinputnopath|
@@ -128,8 +128,9 @@ class InputPaidMedia(TelegramObject):
 
     Args:
         type (:obj:`str`): Type of media that the instance represents.
-        media (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-            :class:`telegram.PhotoSize` | :class:`telegram.Video`): File to send. |fileinputnopath|
+        media (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` | \
+            :class:`pathlib.Path` | :class:`telegram.PhotoSize` | :class:`telegram.Video`): File
+            to send. |fileinputnopath|
             Lastly you can pass an existing telegram media object of the corresponding type
             to send.
 
@@ -167,8 +168,8 @@ class InputPaidMediaPhoto(InputPaidMedia):
     .. versionadded:: 21.4
 
     Args:
-        media (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-            :class:`telegram.PhotoSize`): File to send. |fileinputnopath|
+        media (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` | \
+            :class:`pathlib.Path` | :class:`telegram.PhotoSize`): File to send. |fileinputnopath|
             Lastly you can pass an existing :class:`telegram.PhotoSize` object to send.
 
     Attributes:
@@ -207,8 +208,8 @@ class InputPaidMediaVideo(InputPaidMedia):
            changed by Telegram.
 
     Args:
-        media (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-            :class:`telegram.Video`): File to send. |fileinputnopath|
+        media (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` | \
+            :class:`pathlib.Path` | :class:`telegram.Video`): File to send. |fileinputnopath|
             Lastly you can pass an existing :class:`telegram.Video` object to send.
         thumbnail (:term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | :obj:`str`, \
                 optional): |thumbdocstringnopath|
@@ -278,8 +279,8 @@ class InputMediaAnimation(InputMedia):
       |removed_thumb_note|
 
     Args:
-        media (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-            :class:`telegram.Animation`): File to send. |fileinputnopath|
+        media (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` | \
+            :class:`pathlib.Path` | :class:`telegram.Animation`): File to send. |fileinputnopath|
             Lastly you can pass an existing :class:`telegram.Animation` object to send.
 
             .. versionchanged:: 13.2
@@ -401,8 +402,8 @@ class InputMediaPhoto(InputMedia):
     .. seealso:: :wiki:`Working with Files and Media <Working-with-Files-and-Media>`
 
     Args:
-        media (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-            :class:`telegram.PhotoSize`): File to send. |fileinputnopath|
+        media (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` | \
+            :class:`pathlib.Path` | :class:`telegram.PhotoSize`): File to send. |fileinputnopath|
             Lastly you can pass an existing :class:`telegram.PhotoSize` object to send.
 
             .. versionchanged:: 13.2
@@ -501,8 +502,8 @@ class InputMediaVideo(InputMedia):
       |removed_thumb_note|
 
     Args:
-        media (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-            :class:`telegram.Video`): File to send. |fileinputnopath|
+        media (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` | \
+            :class:`pathlib.Path` | :class:`telegram.Video`): File to send. |fileinputnopath|
             Lastly you can pass an existing :class:`telegram.Video` object to send.
 
             .. versionchanged:: 13.2
@@ -639,8 +640,8 @@ class InputMediaAudio(InputMedia):
       |removed_thumb_note|
 
     Args:
-        media (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-            :class:`telegram.Audio`): File to send. |fileinputnopath|
+        media (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` | \
+            :class:`pathlib.Path` | :class:`telegram.Audio`): File to send. |fileinputnopath|
             Lastly you can pass an existing :class:`telegram.Audio` object to send.
 
             .. versionchanged:: 13.2
@@ -743,8 +744,8 @@ class InputMediaDocument(InputMedia):
       |removed_thumb_note|
 
     Args:
-        media (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path` | \
-            :class:`telegram.Document`): File to send. |fileinputnopath|
+        media (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` \
+            | :class:`pathlib.Path` | :class:`telegram.Document`): File to send. |fileinputnopath|
             Lastly you can pass an existing :class:`telegram.Document` object to send.
 
             .. versionchanged:: 13.2
diff --git a/telegram/_files/inputsticker.py b/telegram/_files/inputsticker.py
index 5539d610d..89f1db81d 100644
--- a/telegram/_files/inputsticker.py
+++ b/telegram/_files/inputsticker.py
@@ -41,7 +41,8 @@ class InputSticker(TelegramObject):
         order of the arguments has changed.
 
     Args:
-        sticker (:obj:`str` | :term:`file object` | :obj:`bytes` | :class:`pathlib.Path`): The
+        sticker (:obj:`str` | :term:`file object` | :class:`~telegram.InputFile` | :obj:`bytes` \
+            | :class:`pathlib.Path`): The
             added sticker. |uploadinputnopath| Animated and video stickers can't be uploaded via
             HTTP URL.
         emoji_list (Sequence[:obj:`str`]): Sequence of
diff --git a/telegram/_utils/files.py b/telegram/_utils/files.py
index 387743025..121c7b339 100644
--- a/telegram/_utils/files.py
+++ b/telegram/_utils/files.py
@@ -61,14 +61,21 @@ def load_file(
     except AttributeError:
         return None, cast(Union[bytes, "InputFile", str, Path], obj)
 
-    if hasattr(obj, "name") and not isinstance(obj.name, int):
-        filename = Path(obj.name).name
-    else:
-        filename = None
+    filename = guess_file_name(obj)
 
     return filename, contents
 
 
+def guess_file_name(obj: FileInput) -> Optional[str]:
+    """If the input is a file handle, read name and return it. Otherwise, return
+    the input unchanged.
+    """
+    if hasattr(obj, "name") and not isinstance(obj.name, int):
+        return Path(obj.name).name
+
+    return None
+
+
 def is_local_file(obj: Optional[FilePathInput]) -> bool:
     """
     Checks if a given string is a file on local system.
@@ -110,8 +117,8 @@ def parse_file_input(  # pylint: disable=too-many-return-statements
       attribute.
 
     Args:
-        file_input (:obj:`str` | :obj:`bytes` | :term:`file object` | Telegram media object): The
-            input to parse.
+        file_input (:obj:`str` | :obj:`bytes` | :term:`file object` | :class:`~telegram.InputFile`\
+            | Telegram media object): The input to parse.
         tg_type (:obj:`type`, optional): The Telegram media type the input can be. E.g.
             :class:`telegram.Animation`.
         filename (:obj:`str`, optional): The filename. Only relevant in case an
diff --git a/telegram/_utils/types.py b/telegram/_utils/types.py
index efde2807f..8a01fdc2d 100644
--- a/telegram/_utils/types.py
+++ b/telegram/_utils/types.py
@@ -82,7 +82,7 @@ ReplyMarkup = Union[
 .. versionadded:: 20.0
 """
 
-FieldTuple = Tuple[str, bytes, str]
+FieldTuple = Tuple[str, Union[bytes, IO[bytes]], str]
 """Alias for return type of `InputFile.field_tuple`."""
 UploadFileDict = Dict[str, FieldTuple]
 """Dictionary containing file data to be uploaded to the API."""
diff --git a/telegram/request/_requestdata.py b/telegram/request/_requestdata.py
index 82d1e3d2c..a6b8752ee 100644
--- a/telegram/request/_requestdata.py
+++ b/telegram/request/_requestdata.py
@@ -129,7 +129,11 @@ class RequestData:
 
     @property
     def multipart_data(self) -> UploadFileDict:
-        """Gives the files contained in this object as mapping of part name to encoded content."""
+        """Gives the files contained in this object as mapping of part name to encoded content.
+
+        .. versionchanged:: NEXT.VERSION
+            Content may now be a file handle.
+        """
         multipart_data: UploadFileDict = {}
         for param in self._parameters:
             m_data = param.multipart_data
diff --git a/telegram/request/_requestparameter.py b/telegram/request/_requestparameter.py
index ab11cbce7..c3d19bdbd 100644
--- a/telegram/request/_requestparameter.py
+++ b/telegram/request/_requestparameter.py
@@ -77,7 +77,11 @@ class RequestParameter:
 
     @property
     def multipart_data(self) -> Optional[UploadFileDict]:
-        """A dict with the file data to upload, if any."""
+        """A dict with the file data to upload, if any.
+
+        .. versionchanged:: NEXT.VERSION
+            Content may now be a file handle.
+        """
         if not self.input_files:
             return None
         return {
diff --git a/tests/_files/test_inputfile.py b/tests/_files/test_inputfile.py
index 1f70cb5cc..b7235497b 100644
--- a/tests/_files/test_inputfile.py
+++ b/tests/_files/test_inputfile.py
@@ -19,7 +19,7 @@
 import contextlib
 import subprocess
 import sys
-from io import BytesIO
+from io import BufferedReader, BytesIO
 
 import pytest
 
@@ -66,21 +66,45 @@ class TestInputFileWithoutRequest:
             assert input_file.attach_name is None
             assert input_file.attach_uri is None
 
-    def test_mimetypes(self):
+    @pytest.mark.parametrize("read_file_handle", [True, False])
+    def test_mimetypes_file_handle(self, read_file_handle):
         # Only test a few to make sure logic works okay
-        assert InputFile(data_file("telegram.jpg").open("rb")).mimetype == "image/jpeg"
+        assert (
+            InputFile(
+                data_file("telegram.jpg").open("rb"), read_file_handle=read_file_handle
+            ).mimetype
+            == "image/jpeg"
+        )
         # For some reason python can guess the type on macOS
-        assert InputFile(data_file("telegram.webp").open("rb")).mimetype in [
+        assert InputFile(
+            data_file("telegram.webp").open("rb"), read_file_handle=read_file_handle
+        ).mimetype in [
             "application/octet-stream",
             "image/webp",
         ]
-        assert InputFile(data_file("telegram.mp3").open("rb")).mimetype == "audio/mpeg"
+        assert (
+            InputFile(
+                data_file("telegram.mp3").open("rb"), read_file_handle=read_file_handle
+            ).mimetype
+            == "audio/mpeg"
+        )
         # For some reason windows drops the trailing i
-        assert InputFile(data_file("telegram.midi").open("rb")).mimetype in [
+        assert InputFile(
+            data_file("telegram.midi").open("rb"), read_file_handle=read_file_handle
+        ).mimetype in [
             "audio/mid",
             "audio/midi",
         ]
 
+        # Test string file
+        assert (
+            InputFile(
+                data_file("text_file.txt").open("rb"), read_file_handle=read_file_handle
+            ).mimetype
+            == "text/plain"
+        )
+
+    def test_mimetypes_other(self):
         # Test guess from file
         assert InputFile(BytesIO(b"blah"), filename="tg.jpg").mimetype == "image/jpeg"
         assert InputFile(BytesIO(b"blah"), filename="tg.mp3").mimetype == "audio/mpeg"
@@ -92,20 +116,49 @@ class TestInputFileWithoutRequest:
         )
         assert InputFile(BytesIO(b"blah")).mimetype == "application/octet-stream"
 
-        # Test string file
-        assert InputFile(data_file("text_file.txt").open()).mimetype == "text/plain"
-
-    def test_filenames(self):
-        assert InputFile(data_file("telegram.jpg").open("rb")).filename == "telegram.jpg"
-        assert InputFile(data_file("telegram.jpg").open("rb"), filename="blah").filename == "blah"
+    @pytest.mark.parametrize("read_file_handle", [True, False])
+    def test_filenames(self, read_file_handle):
         assert (
-            InputFile(data_file("telegram.jpg").open("rb"), filename="blah.jpg").filename
+            InputFile(
+                data_file("telegram.jpg").open("rb"), read_file_handle=read_file_handle
+            ).filename
+            == "telegram.jpg"
+        )
+        assert (
+            InputFile(
+                data_file("telegram.jpg").open("rb"),
+                filename="blah",
+                read_file_handle=read_file_handle,
+            ).filename
+            == "blah"
+        )
+        assert (
+            InputFile(
+                data_file("telegram.jpg").open("rb"),
+                filename="blah.jpg",
+                read_file_handle=read_file_handle,
+            ).filename
             == "blah.jpg"
         )
-        assert InputFile(data_file("telegram").open("rb")).filename == "telegram"
-        assert InputFile(data_file("telegram").open("rb"), filename="blah").filename == "blah"
         assert (
-            InputFile(data_file("telegram").open("rb"), filename="blah.jpg").filename == "blah.jpg"
+            InputFile(data_file("telegram").open("rb"), read_file_handle=read_file_handle).filename
+            == "telegram"
+        )
+        assert (
+            InputFile(
+                data_file("telegram").open("rb"),
+                filename="blah",
+                read_file_handle=read_file_handle,
+            ).filename
+            == "blah"
+        )
+        assert (
+            InputFile(
+                data_file("telegram").open("rb"),
+                filename="blah.jpg",
+                read_file_handle=read_file_handle,
+            ).filename
+            == "blah.jpg"
         )
 
         class MockedFileobject:
@@ -140,6 +193,19 @@ class TestInputFileWithoutRequest:
             == "blah.jpg"
         )
 
+    @pytest.mark.parametrize("read_file_handle", [True, False])
+    def test_read_file_handle(self, read_file_handle):
+        input_file = InputFile(
+            data_file("telegram.jpg").open("rb"), read_file_handle=read_file_handle
+        )
+        content = input_file.field_tuple[1]
+        if read_file_handle:
+            assert isinstance(content, bytes)
+            assert content == data_file("telegram.jpg").read_bytes()
+        else:
+            assert isinstance(content, BufferedReader)
+            assert content.read() == data_file("telegram.jpg").read_bytes()
+
 
 class TestInputFileWithRequest:
     async def test_send_bytes(self, bot, chat_id):
diff --git a/tests/request/test_request.py b/tests/request/test_request.py
index 55100940b..9ce5ee286 100644
--- a/tests/request/test_request.py
+++ b/tests/request/test_request.py
@@ -30,6 +30,7 @@ import httpx
 import pytest
 from httpx import AsyncHTTPTransport
 
+from telegram import InputFile
 from telegram._utils.defaultvalue import DEFAULT_NONE
 from telegram._utils.strings import TextEncoding
 from telegram.error import (
@@ -48,6 +49,7 @@ from telegram.request._httpxrequest import HTTPXRequest
 from telegram.request._requestparameter import RequestParameter
 from telegram.warnings import PTBDeprecationWarning
 from tests.auxil.envvars import TEST_WITH_OPT_DEPS
+from tests.auxil.files import data_file
 from tests.auxil.networking import NonchalantHttpxRequest
 from tests.auxil.slots import mro_slots
 
@@ -821,3 +823,15 @@ class TestHTTPXRequestWithRequest:
             task_2.exception()
         except (asyncio.CancelledError, asyncio.InvalidStateError):
             pass
+
+    async def test_input_file_postponed_read(self, bot, chat_id):
+        """Here we test that `read_file_handle=False` is correctly handled by HTTPXRequest.
+        Since manually building the RequestData object has no real benefit, we simply use the Bot
+        for that.
+        """
+        message = await bot.send_document(
+            document=InputFile(data_file("telegram.jpg").open("rb"), read_file_handle=False),
+            chat_id=chat_id,
+        )
+        assert message.document
+        assert message.document.file_name == "telegram.jpg"
diff --git a/tests/test_official/exceptions.py b/tests/test_official/exceptions.py
index c9e3b4e46..c6122f312 100644
--- a/tests/test_official/exceptions.py
+++ b/tests/test_official/exceptions.py
@@ -117,7 +117,7 @@ PTB_EXTRA_PARAMS = {
     "PassportElementError": {"source", "type", "message"},
     "InputMedia": {"caption", "caption_entities", "media", "media_type", "parse_mode"},
     "InputMedia(Animation|Audio|Document|Photo|Video|VideoNote|Voice)": {"filename"},
-    "InputFile": {"attach", "filename", "obj"},
+    "InputFile": {"attach", "filename", "obj", "read_file_handle"},
     "MaybeInaccessibleMessage": {"date", "message_id", "chat"},  # attributes common to all subcls
     "ChatBoostSource": {"source"},  # attributes common to all subclasses
     "MessageOrigin": {"type", "date"},  # attributes common to all subclasses