diff --git a/django/core/handlers/wsgi.py b/django/core/handlers/wsgi.py
index bca0857622..c071b5ca8c 100644
--- a/django/core/handlers/wsgi.py
+++ b/django/core/handlers/wsgi.py
@@ -1,4 +1,4 @@
-from io import BytesIO
+from io import IOBase
 
 from django.conf import settings
 from django.core import signals
@@ -12,55 +12,45 @@ from django.utils.regex_helper import _lazy_re_compile
 _slashes_re = _lazy_re_compile(rb"/+")
 
 
-class LimitedStream:
-    """Wrap another stream to disallow reading it past a number of bytes."""
+class LimitedStream(IOBase):
+    """
+    Wrap another stream to disallow reading it past a number of bytes.
+
+    Based on the implementation from werkzeug.wsgi.LimitedStream
+    See https://github.com/pallets/werkzeug/blob/dbf78f67/src/werkzeug/wsgi.py#L828
+    """
 
     def __init__(self, stream, limit):
-        self.stream = stream
-        self.remaining = limit
-        self.buffer = b""
+        self._read = stream.read
+        self._readline = stream.readline
+        self._pos = 0
+        self.limit = limit
 
-    def _read_limited(self, size=None):
-        if size is None or size > self.remaining:
-            size = self.remaining
-        if size == 0:
+    def read(self, size=-1, /):
+        _pos = self._pos
+        limit = self.limit
+        if _pos >= limit:
             return b""
-        result = self.stream.read(size)
-        self.remaining -= len(result)
-        return result
-
-    def read(self, size=None):
-        if size is None:
-            result = self.buffer + self._read_limited()
-            self.buffer = b""
-        elif size < len(self.buffer):
-            result = self.buffer[:size]
-            self.buffer = self.buffer[size:]
-        else:  # size >= len(self.buffer)
-            result = self.buffer + self._read_limited(size - len(self.buffer))
-            self.buffer = b""
-        return result
-
-    def readline(self, size=None):
-        while b"\n" not in self.buffer and (size is None or len(self.buffer) < size):
-            if size:
-                # since size is not None here, len(self.buffer) < size
-                chunk = self._read_limited(size - len(self.buffer))
-            else:
-                chunk = self._read_limited()
-            if not chunk:
-                break
-            self.buffer += chunk
-        sio = BytesIO(self.buffer)
-        if size:
-            line = sio.readline(size)
+        if size == -1 or size is None:
+            size = limit - _pos
         else:
-            line = sio.readline()
-        self.buffer = sio.read()
-        return line
+            size = min(size, limit - _pos)
+        data = self._read(size)
+        self._pos += len(data)
+        return data
 
-    def close(self):
-        pass
+    def readline(self, size=-1, /):
+        _pos = self._pos
+        limit = self.limit
+        if _pos >= limit:
+            return b""
+        if size == -1 or size is None:
+            size = limit - _pos
+        else:
+            size = min(size, limit - _pos)
+        line = self._readline(size)
+        self._pos += len(line)
+        return line
 
 
 class WSGIRequest(HttpRequest):
diff --git a/django/core/servers/basehttp.py b/django/core/servers/basehttp.py
index 74a42966a6..fef5532e58 100644
--- a/django/core/servers/basehttp.py
+++ b/django/core/servers/basehttp.py
@@ -144,7 +144,7 @@ class ServerHandler(simple_server.ServerHandler):
             self.request_handler.close_connection = True
 
     def close(self):
-        self.get_stdin()._read_limited()
+        self.get_stdin().read()
         super().close()
 
 
diff --git a/docs/releases/4.2.txt b/docs/releases/4.2.txt
index 39235aa224..68392161e3 100644
--- a/docs/releases/4.2.txt
+++ b/docs/releases/4.2.txt
@@ -523,6 +523,10 @@ Miscellaneous
 
 .. _`redis-py`: https://pypi.org/project/redis/
 
+* Manually instantiated ``WSGIRequest`` objects must be provided a file-like
+  object for ``wsgi.input``. Previously, Django was more lax than the expected
+  behavior as specified by the WSGI specification.
+
 .. _deprecated-features-4.2:
 
 Features deprecated in 4.2
diff --git a/tests/builtin_server/tests.py b/tests/builtin_server/tests.py
index 2777db1e13..f654fdd92c 100644
--- a/tests/builtin_server/tests.py
+++ b/tests/builtin_server/tests.py
@@ -81,7 +81,7 @@ class WSGIFileWrapperTests(TestCase):
 
     def test_file_wrapper_uses_sendfile(self):
         env = {"SERVER_PROTOCOL": "HTTP/1.0"}
-        handler = FileWrapperHandler(None, BytesIO(), BytesIO(), env)
+        handler = FileWrapperHandler(BytesIO(), BytesIO(), BytesIO(), env)
         handler.run(wsgi_app_file_wrapper)
         self.assertTrue(handler._used_sendfile)
         self.assertEqual(handler.stdout.getvalue(), b"")
@@ -89,7 +89,7 @@ class WSGIFileWrapperTests(TestCase):
 
     def test_file_wrapper_no_sendfile(self):
         env = {"SERVER_PROTOCOL": "HTTP/1.0"}
-        handler = FileWrapperHandler(None, BytesIO(), BytesIO(), env)
+        handler = FileWrapperHandler(BytesIO(), BytesIO(), BytesIO(), env)
         handler.run(wsgi_app)
         self.assertFalse(handler._used_sendfile)
         self.assertEqual(handler.stdout.getvalue().splitlines()[-1], b"Hello World!")
@@ -102,7 +102,7 @@ class WSGIFileWrapperTests(TestCase):
         response when file_wrapper is used.
         """
         env = RequestFactory().get("/fileresponse/").environ
-        handler = FileWrapperHandler(None, BytesIO(), BytesIO(), env)
+        handler = FileWrapperHandler(BytesIO(), BytesIO(), BytesIO(), env)
         handler.run(get_internal_wsgi_application())
         # Sendfile is used only when file_wrapper has been used.
         self.assertTrue(handler._used_sendfile)
@@ -119,7 +119,7 @@ class WSGIFileWrapperTests(TestCase):
     @override_settings(ROOT_URLCONF="builtin_server.urls")
     def test_file_response_call_request_finished(self):
         env = RequestFactory().get("/fileresponse/").environ
-        handler = FileWrapperHandler(None, BytesIO(), BytesIO(), env)
+        handler = FileWrapperHandler(BytesIO(), BytesIO(), BytesIO(), env)
         with mock.MagicMock() as signal_handler:
             request_finished.connect(signal_handler)
             handler.run(get_internal_wsgi_application())