--- a/tools/lint/docs/linters/flake8.rst
+++ b/tools/lint/docs/linters/flake8.rst
@@ -30,15 +30,21 @@ in a source directory, it must be added 
 If you wish to exclude a subdirectory of an included one, you can add it to the ``exclude``
 directive.
 
 The default configuration file lives in ``topsrcdir/.flake8``. The default configuration can be
 overriden for a given subdirectory by creating a new ``.flake8`` file in the subdirectory. Be warned
 that ``.flake8`` files cannot inherit from one another, so all configuration you wish to keep must
 be re-defined.
 
+.. warning::
+
+    Only ``.flake8`` files that live in a directory that is explicitly included in the ``include``
+    directive will be considered. See `bug 1277851`_ for more details.
+
 For an overview of the supported configuration, see `flake8's documentation`_.
 
 .. _Flake8: https://flake8.readthedocs.io/en/latest/
 .. _pep8: http://pep8.readthedocs.io/en/latest/
 .. _pyflakes: https://github.com/pyflakes/pyflakes
 .. _mccabe: https://github.com/pycqa/mccabe
+.. _bug 1277851: https://bugzilla.mozilla.org/show_bug.cgi?id=1277851
 .. _flake8's documentation: https://flake8.readthedocs.io/en/latest/config.html

--- a/tools/lint/flake8.lint
+++ b/tools/lint/flake8.lint
@@ -59,16 +59,31 @@ def process_line(line):
             res['level'] = 'warning'
 
         if res['code'] in LINE_OFFSETS:
             res['lineoffset'] = LINE_OFFSETS[res['code']]
 
     results.append(result.from_linter(LINTER, **res))
 
 
+def run_process(cmdargs):
+    # flake8 seems to handle SIGINT poorly. Handle it here instead
+    # so we can kill the process without a cryptic traceback.
+    orig = signal.signal(signal.SIGINT, signal.SIG_IGN)
+    proc = ProcessHandler(cmdargs, env=os.environ,
+                          processOutputLine=process_line)
+    proc.run()
+    signal.signal(signal.SIGINT, orig)
+
+    try:
+        proc.wait()
+    except KeyboardInterrupt:
+        proc.kill()
+
+
 def lint(files, **lintargs):
     binary = os.environ.get('FLAKE8')
     if not binary:
         try:
             binary = which.which('flake8')
         except which.WhichError:
             pass
 
@@ -81,30 +96,29 @@ def lint(files, **lintargs):
         '--format', '{"path":"%(path)s","lineno":%(row)s,'
                     '"column":%(col)s,"rule":"%(code)s","message":"%(text)s"}',
     ]
 
     exclude = lintargs.get('exclude')
     if exclude:
         cmdargs += ['--exclude', ','.join(lintargs['exclude'])]
 
-    cmdargs += files
+    # Run any paths with a .flake8 file in the directory separately so
+    # it gets picked up. This means only .flake8 files that live in
+    # directories that are explicitly included will be considered.
+    # See bug 1277851
+    no_config = []
+    for f in files:
+        if not os.path.isfile(os.path.join(f, '.flake8')):
+            no_config.append(f)
+            continue
+        run_process(cmdargs+[f])
 
-    # flake8 seems to handle SIGINT poorly. Handle it here instead
-    # so we can kill the process without a cryptic traceback.
-    orig = signal.signal(signal.SIGINT, signal.SIG_IGN)
-    proc = ProcessHandler(cmdargs, env=os.environ,
-                          processOutputLine=process_line)
-    proc.run()
-    signal.signal(signal.SIGINT, orig)
-
-    try:
-        proc.wait()
-    except KeyboardInterrupt:
-        proc.kill()
+    if no_config:
+        run_process(cmdargs+no_config)
 
     return results
 
 
 LINTER = {
     'name': "flake8",
     'description': "Python linter",
     'include': [