diff --git a/.flake8 b/.flake8
index 6ab1219ead..b5eec11702 100644
--- a/.flake8
+++ b/.flake8
@@ -138,7 +138,7 @@ per-file-ignores =
   cheroot/test/conftest.py: DAR101, DAR201, DAR301, I001, I003, I005, WPS100, WPS130, WPS325, WPS354, WPS420, WPS422, WPS430, WPS457
   cheroot/test/helper.py: DAR101, DAR201, DAR401, I001, I003, I004, N802, WPS110, WPS111, WPS121, WPS201, WPS220, WPS231, WPS301, WPS414, WPS421, WPS422, WPS505
   cheroot/test/test_cli.py: DAR101, DAR201, I001, I005, N802, S101, S108, WPS110, WPS421, WPS431, WPS473
-  cheroot/test/test_makefile.py: DAR101, DAR201, I004, RST304, S101, WPS110, WPS122
+  cheroot/test/test_makefile.py: DAR101, DAR201, DAR401, I004, RST304, S101, WPS110, WPS122, WPS202
   cheroot/test/test_wsgi.py: DAR101, DAR301, I001, I004, S101, WPS110, WPS111, WPS117, WPS118, WPS121, WPS210, WPS421, WPS430, WPS432, WPS441, WPS509
   cheroot/test/test_core.py: C815, DAR101, DAR201, DAR401, I003, I004, N805, N806, S101, WPS110, WPS111, WPS114, WPS121, WPS202, WPS204, WPS226, WPS229, WPS324, WPS421, WPS422, WPS432, WPS602
   cheroot/test/test_dispatch.py: DAR101, DAR201, S101, WPS111, WPS121, WPS422, WPS430
diff --git a/cheroot/errors.py b/cheroot/errors.py
index a1103595c2..a65e641aa8 100644
--- a/cheroot/errors.py
+++ b/cheroot/errors.py
@@ -3,6 +3,8 @@
 import errno
 import sys
 
+from . import _compat
+
 
 class MaxSizeExceeded(Exception):
     """Exception raised when a client sends more data then allowed under limit.
@@ -66,6 +68,10 @@ def plat_specific_errors(*errnames):
 
 
 acceptable_sock_shutdown_error_codes = {
+    errno.EBADF,  # operating on a closed/invalid file descriptor
+    *(
+        (errno.WSAENOTSOCK,) if _compat.IS_WINDOWS else ()
+    ),  # Windows equivalent of EBADF
     errno.ENOTCONN,
     errno.EPIPE,
     errno.ESHUTDOWN,  # corresponds to BrokenPipeError in Python 3
@@ -73,12 +79,16 @@ def plat_specific_errors(*errnames):
 }
 """Errors that may happen during the connection close sequence.
 
+* EBADF — operating on a closed or invalid file descriptor
+* WSAENOTSOCK — Windows equivalent of EBADF; raised when the socket has
+  already been closed by the OS or another thread
 * ENOTCONN — client is no longer connected
 * EPIPE — write on a pipe while the other end has been closed
 * ESHUTDOWN — write on a socket which has been shutdown for writing
 * ECONNRESET — connection is reset by the peer, we received a TCP RST packet
 
 Refs:
+
 * https://github.com/cherrypy/cheroot/issues/341#issuecomment-735884889
 * https://bugs.python.org/issue30319
 * https://bugs.python.org/issue30329
@@ -87,4 +97,8 @@ def plat_specific_errors(*errnames):
 * https://docs.microsoft.com/windows/win32/api/winsock/nf-winsock-shutdown
 """
 
-acceptable_sock_shutdown_exceptions = (BrokenPipeError, ConnectionResetError)
+
+acceptable_sock_shutdown_exceptions = (
+    BrokenPipeError,  # Covers EPIPE and ESHUTDOWN
+    ConnectionResetError,  # Covers ECONNRESET
+)
diff --git a/cheroot/errors.pyi b/cheroot/errors.pyi
index dd60f7a4a4..e5fc96a97c 100644
--- a/cheroot/errors.pyi
+++ b/cheroot/errors.pyi
@@ -1,5 +1,3 @@
-import typing as _t
-
 class MaxSizeExceeded(Exception): ...
 class NoSSLError(Exception): ...
 class FatalSSLAlert(Exception): ...
@@ -10,4 +8,7 @@ socket_error_eintr: list[int]
 socket_errors_to_ignore: list[int]
 socket_errors_nonblocking: list[int]
 acceptable_sock_shutdown_error_codes: set[int]
-acceptable_sock_shutdown_exceptions: tuple[_t.Type[Exception], ...]
+acceptable_sock_shutdown_exceptions: tuple[
+    type[BrokenPipeError],
+    type[ConnectionResetError],
+]
diff --git a/cheroot/makefile.py b/cheroot/makefile.py
index f5780a1ede..d3d40682de 100644
--- a/cheroot/makefile.py
+++ b/cheroot/makefile.py
@@ -4,6 +4,8 @@
 import _pyio as io
 import socket
 
+from . import errors as _errors
+
 
 # Write only 16K at a time to sockets
 SOCK_WRITE_BLOCKSIZE = 16384
@@ -32,8 +34,45 @@ def _flush_unlocked(self):
                 n = self.raw.write(bytes(self._write_buf))
             except io.BlockingIOError as e:
                 n = e.characters_written
+
+            if n == 0:
+                # Non-blocking socket can't write right now — stop flushing.
+                break
+            if not n:
+                # Defensive: write() returned None or other falsy value,
+                # which shouldn't happen but could cause an infinite loop.
+                break
+
             del self._write_buf[:n]
 
+    def close(self):
+        """
+        Close the stream and its underlying file object.
+
+        This method is designed to be idempotent (it can be called multiple
+        times without side effects). It gracefully handles a race condition
+        where the underlying socket may have already been closed by the remote
+        client or another thread.
+
+        A :exc:`ConnectionError` or :exc:`OSError` with
+        :data:`~errno.EBADF` or :data:`~errno.ENOTCONN` is caught
+        and ignored, as these indicate a normal, expected connection teardown.
+        Other exceptions are re-raised.
+        """
+        # pylint incorrectly flags inherited self.closed property as constant
+        if self.closed:  # pylint: disable=using-constant-test
+            return
+
+        try:
+            super().close()
+        except ConnectionError:
+            return
+        except OSError as err:
+            # Handle EBADF and other acceptable socket shutdown errors
+            if err.errno in _errors.acceptable_sock_shutdown_error_codes:
+                return
+            raise
+
 
 class StreamReader(io.BufferedReader):
     """Socket stream reader."""
diff --git a/cheroot/test/test_makefile.py b/cheroot/test/test_makefile.py
index d65d4ea268..2207ae696c 100644
--- a/cheroot/test/test_makefile.py
+++ b/cheroot/test/test_makefile.py
@@ -1,10 +1,16 @@
 """Tests for :py:mod:`cheroot.makefile`."""
 
+import _pyio
+import errno
+import io
+
+import pytest
+
 from cheroot import makefile
 
 
 class MockSocket:
-    """A mock socket."""
+    """A mock socket for emulating buffered I/O."""
 
     def __init__(self):
         """Initialize :py:class:`MockSocket`."""
@@ -35,6 +41,31 @@ def _decref_socketios(self):
         # Ref: https://github.com/cherrypy/cheroot/issues/734
 
 
+class MockRawIO:
+    """A mock ``io.RawIOBase`` object for use as the raw layer of a ``BufferedWriter``."""
+
+    def __init__(self):
+        """Initialize :py:class:`MockRawIO`."""
+        self._is_closed = False
+
+    def write(self, message):
+        """Emulate ``io.RawIOBase write``."""
+        return len(message)
+
+    def writable(self):
+        """Indicate that the raw stream supports writing."""
+        return True
+
+    def close(self):
+        """Emulate close."""
+        self._is_closed = True
+
+    @property
+    def closed(self):
+        """Emulate the required ``closed`` property."""
+        return self._is_closed
+
+
 def test_bytes_read():
     """Reader should capture bytes read."""
     sock = MockSocket()
@@ -51,3 +82,78 @@ def test_bytes_written():
     wfile = makefile.MakeFile(sock, 'w')
     wfile.write(b'bar')
     assert wfile.bytes_written == 3
+
+
+def test_close_is_idempotent():
+    """Test that double ``close()`` does not error out."""
+    raw_buffer = io.BytesIO()
+    buffered_writer = makefile.BufferedWriter(raw_buffer)
+
+    buffered_writer.close()
+    assert buffered_writer.closed
+
+    buffered_writer.close()
+    assert buffered_writer.closed
+
+
+def test_close_when_raw_already_closed():
+    """Test that ``close()`` is safe when the raw buffer was closed externally.
+
+    Simulates a race where the OS or another thread closed the raw socket
+    before ``BufferedWriter.close()`` is called.
+    """
+    raw_buffer = io.BytesIO()
+    buffered_writer = makefile.BufferedWriter(raw_buffer)
+
+    raw_buffer.close()
+    assert buffered_writer.closed  # property reflects raw state
+
+    buffered_writer.close()
+
+
+@pytest.mark.parametrize(
+    ('exc', 'reraises'),
+    (
+        (BrokenPipeError(errno.EPIPE, 'Broken pipe'), False),
+        (OSError(errno.EBADF, 'Bad file descriptor'), False),
+        (OSError(errno.EIO, 'I/O error'), True),
+    ),
+    ids=['broken_pipe', 'ebadf', 'unexpected_oserror'],
+)
+def test_close_error_handling(exc, reraises, mocker):
+    """Test that expected socket errors are swallowed and others re-raised."""
+    writer = makefile.BufferedWriter(MockRawIO())
+    mocker.patch.object(_pyio.BufferedWriter, 'close', side_effect=exc)
+    if reraises:
+        with pytest.raises(OSError, match='I/O error'):
+            writer.close()
+    else:
+        writer.close()
+
+
+def _make_blocking_io_error():
+    """Create a :exc:`BlockingIOError` with ``characters_written`` set."""
+    err = io.BlockingIOError(errno.EAGAIN, 'Resource temporarily unavailable')
+    err.characters_written = 5
+    return err
+
+
+@pytest.mark.parametrize(
+    ('write_kwargs', 'expected_buf_len'),
+    (
+        ({'return_value': 0}, len(b'data to flush')),
+        ({'return_value': None}, len(b'data to flush')),
+        ({'side_effect': _make_blocking_io_error()}, 0),
+    ),
+    ids=['zero_return', 'none_return', 'blocking_io_error'],
+)
+def test_flush_unlocked_write_outcomes(write_kwargs, expected_buf_len, mocker):
+    """Test that ``_flush_unlocked`` handles various ``write()`` outcomes."""
+    data = b'data to flush'
+    writer = makefile.BufferedWriter(MockRawIO())
+    writer._write_buf = bytearray(data)
+    mocker.patch.object(writer.raw, 'write', **write_kwargs)
+
+    writer._flush_unlocked()
+
+    assert len(writer._write_buf) == expected_buf_len
diff --git a/docs/changelog-fragments.d/779.bugfix.rst b/docs/changelog-fragments.d/779.bugfix.rst
new file mode 100644
index 0000000000..615d08368b
--- /dev/null
+++ b/docs/changelog-fragments.d/779.bugfix.rst
@@ -0,0 +1,4 @@
+Socket I/O is now resilient to race conditions happening during connection teardown
+due to sockets dying independently or being closed externally.
+
+-- by :user:`julianz-`
diff --git a/docs/spelling_wordlist.txt b/docs/spelling_wordlist.txt
index 06b204518e..5305595e22 100644
--- a/docs/spelling_wordlist.txt
+++ b/docs/spelling_wordlist.txt
@@ -67,6 +67,7 @@ subpackages
 symlinked
 syscall
 systemd
+teardown
 threadpool
 Tidelift
 TLS