diff --git a/pkgs/by-name/ni/nixos-rebuild-ng/src/nixos_rebuild/process.py b/pkgs/by-name/ni/nixos-rebuild-ng/src/nixos_rebuild/process.py
index d848709ef8f1..7ba809d4cb9c 100644
--- a/pkgs/by-name/ni/nixos-rebuild-ng/src/nixos_rebuild/process.py
+++ b/pkgs/by-name/ni/nixos-rebuild-ng/src/nixos_rebuild/process.py
@@ -25,7 +25,7 @@ SSH_DEFAULT_OPTS: Final = [
     "-o",
     "ControlMaster=auto",
     "-o",
-    f"ControlPath={tmpdir.TMPDIR_PATH / 'ssh-%C'}",
+    f"ControlPath={tmpdir.SSH_CONTROL_PATH}",
     "-o",
     "ControlPersist=60",
 ]
diff --git a/pkgs/by-name/ni/nixos-rebuild-ng/src/nixos_rebuild/tmpdir.py b/pkgs/by-name/ni/nixos-rebuild-ng/src/nixos_rebuild/tmpdir.py
index 9db6e310a4d2..1df30dcad7eb 100644
--- a/pkgs/by-name/ni/nixos-rebuild-ng/src/nixos_rebuild/tmpdir.py
+++ b/pkgs/by-name/ni/nixos-rebuild-ng/src/nixos_rebuild/tmpdir.py
@@ -1,38 +1,86 @@
 import logging
+import os
 from pathlib import Path
-from tempfile import TemporaryDirectory, gettempdir
+from tempfile import TemporaryDirectory
 from typing import Final
 
 logger: Final = logging.getLogger(__name__)
 
+# The Linux kernel hardcodes a limit of 108 bytes for Unix sockets [0],
+# but that includes one NULL byte at the very end, so the logical max
+# length is 107 bytes.
+# [0]: https://git.kernel.org/pub/scm/linux/kernel/git/stable/linux.git/tree/include/uapi/linux/un.h?h=v6.18.37#n7
+LINUX_MAX_SOCKET_LENGTH: Final = 107
 
-# Very long tmp dirs lead to "too long for Unix domain socket"
-# SSH ControlPath errors. Especially macOS sets long TMPDIR paths.
-# This is also required for Linux, if the user tries to build
-# from inside a shell using `--target-host`, which will cause
-# ssh to fail with "ControlPath too long"
+# OpenSSH expands %C to `conn_hash_hex` [0],
+# which is the result of calling `ssh_connection_hash` [1],
+# which computes a sha1 digest [2],
+# which is 20 bytes long [3].
+# which gets hex encoded [4] to double that length [5].
 #
-# The constant is based on a worst case example FQDN, e.g.:
-# `ec2-123-123-123-123.ap-southeast-2.compute.amazonaws.com` (56 bytes).
-# The `ControlPath` can maximum be 108 bytes. Given the prefix
-# that is used for the tempdir, ie. `nixos-rebuild.47i6dz8c` (22 bytes),
-# we have 30 bytes left to work with.
-# This should be fine for the usual temp folders:
-# /tmp/tmp.7hBqN2Fm5H (19)
-# /var/tmp/tmp.7hBqN2Fm5H (23)
-# /run/user/1000/tmp.7hBqN2Fm5H (29)
+# [0]: https://github.com/openssh/openssh-portable/blob/V_10_3_P1/sshconnect.h#L70
+# [1]: https://github.com/openssh/openssh-portable/blob/V_10_3_P1/ssh.c#L1464-L1465
+# [2]: https://github.com/openssh/openssh-portable/blob/V_10_3_P1/readconf.c#L345
+# [3]: https://github.com/openssh/openssh-portable/blob/V_10_3_P1/openbsd-compat/sha1.h#L15
+# [4]: https://github.com/openssh/openssh-portable/blob/V_10_3_P1/readconf.c#L360
+# [5]: https://github.com/openssh/openssh-portable/blob/V_10_3_P1/misc.c#L1627
+OPENSSH_PERCENT_C_LENGTH: Final = 40
+
+# OpenSSH adds a suffix to the given control path [0].
+# There's 1 character for a `.` separator, followed by 16 random characters [1].
+# [0]: https://github.com/openssh/openssh-portable/blob/V_10_3_P1/mux.c#L1348
+# [1]: https://github.com/openssh/openssh-portable/blob/V_10_3_P1/mux.c#L1324
+OPENSSH_CONTROL_PATH_SUFFIX_LENGTH: Final = 1 + 16
+
+# Carefully compute a maximum allowed length for a tmpdir, otherwise ssh crashes with errors like this:
+# > unix_listener: path "/home/runner/work/_temp/nixos-rebuild.aw8hzmq7/ssh-ea7c10de83787b1dec3f06ef20ee26b38c6bb0a5.x9MDykk4gmASsl3R"
+# > too long for Unix domain socket
+#
+# The full path to our tmpdir must be short enough for the resulting Unix domain
+# sockets that OpenSSH creates to fit within `LINUX_MAX_SOCKET_LENGTH`.
+# It's common for system configured temp dirs to be more
+# than a few characters:
+# - macOS sets long TMPDIR paths.
+# - Nix dev shells set a longer TMPDIR
+# - GitHub actions set TMPDIR to something like `/home/runner/work/_temp`.
+#
+# Breaking down the socket path into its component pieces:
+#
+# /home/runner/work/_temp/nixos-rebuild.aw8hzmq7/ssh-ea7c10de83787b1dec3f06ef20ee26b38c6bb0a5.x9MDykk4gmASsl3R
+# |-------------- TMPDIR ----------------------|^|----------------- ssh-%C -----------------||---------------|
+#                                               |                                                   |
+#                                Note the path separator character.                   OPENSSH_CONTROL_PATH_SUFFIX_LENGTH
+#
+MAX_TMPDIR_LENGTH: Final = (
+    LINUX_MAX_SOCKET_LENGTH
+    - 1  # Path separator between tmpdir and the socket name.
+    # Keep the following in sync with `SSH_CONTROL_PATH`.
+    - len("ssh-")
+    - OPENSSH_PERCENT_C_LENGTH
+    - OPENSSH_CONTROL_PATH_SUFFIX_LENGTH
+)
+
+
 def make_tmpdir() -> TemporaryDirectory[str]:
-    tmp = gettempdir()
-    if len(tmp) >= 30:
+    prefix = "nixos-rebuild."
+    tmpdir = TemporaryDirectory(prefix=prefix)
+    if len(os.fsencode(tmpdir.name)) > MAX_TMPDIR_LENGTH:
+        short_tmpdir = TemporaryDirectory(prefix=prefix, dir="/tmp")
         logger.debug(
-            "tempdir '%s' exceeds 30 bytes limit, defaulting to /tmp instead",
-            tmp,
+            "tempdir '%s' exceeds %s bytes limit, defaulting to '%s' instead",
+            tmpdir,
+            MAX_TMPDIR_LENGTH,
+            short_tmpdir,
         )
 
-        return TemporaryDirectory(prefix="nixos-rebuild.", dir="/tmp")
+        tmpdir.cleanup()
+        return short_tmpdir
 
-    return TemporaryDirectory(prefix="nixos-rebuild.")
+    return tmpdir
 
 
 TMPDIR: Final = make_tmpdir()
 TMPDIR_PATH: Final = Path(TMPDIR.name)
+
+# Keep this in sync with `MAX_TMPDIR_LENGTH`!
+SSH_CONTROL_PATH: Final = str(TMPDIR_PATH / "ssh-%C")
diff --git a/pkgs/by-name/ni/nixos-rebuild-ng/src/tests/test_tmpdir.py b/pkgs/by-name/ni/nixos-rebuild-ng/src/tests/test_tmpdir.py
new file mode 100644
index 000000000000..5735e7b979f3
--- /dev/null
+++ b/pkgs/by-name/ni/nixos-rebuild-ng/src/tests/test_tmpdir.py
@@ -0,0 +1,56 @@
+import contextlib
+import os
+import tempfile
+import typing
+from pathlib import Path
+
+from nixos_rebuild.tmpdir import MAX_TMPDIR_LENGTH, make_tmpdir
+
+
+@contextlib.contextmanager
+def system_tempdir(path: Path) -> typing.Generator[None]:
+    path.mkdir(exist_ok=True)
+
+    # `tempfile` caches the tempdir, you must clear it for it to recompute.
+    tempfile.tempdir = None
+
+    og_tmpdir = os.environ.get("TMPDIR")
+
+    try:
+        os.environ["TMPDIR"] = str(path)
+        assert Path(tempfile.gettempdir()) == path
+        yield
+    finally:
+        if og_tmpdir is None:
+            del os.environ["TMPDIR"]
+        else:
+            os.environ["TMPDIR"] = og_tmpdir
+
+
+def test_make_tmpdir() -> None:
+    # Basic test: whatever the default system temp dir happens to be.
+    tmpdir = make_tmpdir()
+    tmp = Path(tmpdir.name)
+    assert tmp.exists()
+    assert tmp.is_dir()
+    assert len(os.fsencode(str(tmp))) <= MAX_TMPDIR_LENGTH
+
+    # Test with a short system temp dir. We should use it unmodified.
+    with system_tempdir(Path("/tmp/not-too-long")):
+        tmpdir = make_tmpdir()
+        tmp = Path(tmpdir.name)
+
+        assert tmp.exists()
+        assert tmp.is_dir()
+        assert len(os.fsencode(str(tmp))) <= MAX_TMPDIR_LENGTH
+
+    # Test with a long system temp dir. We should ignore
+    # it and fall back to something short enough for OpenSSH to
+    # create sockets in.
+    with system_tempdir(Path("/tmp/long" + ("g" * MAX_TMPDIR_LENGTH))):
+        tmpdir = make_tmpdir()
+        tmp = Path(tmpdir.name)
+
+        assert tmp.exists()
+        assert tmp.is_dir()
+        assert len(os.fsencode(str(tmp))) <= MAX_TMPDIR_LENGTH