--- a/tools/lint/python/flake8.py
+++ b/tools/lint/python/flake8.py
@@ -1,19 +1,20 @@
 # This Source Code Form is subject to the terms of the Mozilla Public
 # License, v. 2.0. If a copy of the MPL was not distributed with this
 # file, You can obtain one at http://mozilla.org/MPL/2.0/.
 
 import json
 import os
+import platform
 import signal
 import subprocess
+import sys
 from collections import defaultdict
 
-import which
 from mozprocess import ProcessHandlerMixin
 
 from mozlint import result
 from mozlint.pathutils import get_ancestors_by_name
 
 
 here = os.path.abspath(os.path.dirname(__file__))
 FLAKE8_REQUIREMENTS_PATH = os.path.join(here, 'flake8_requirements.txt')
@@ -50,16 +51,23 @@ LINE_OFFSETS = {
     'E302': (-2, 3),
 }
 """Maps a flake8 error to a lineoffset tuple.
 
 The offset is of the form (lineno_offset, num_lines) and is passed
 to the lineoffset property of `ResultContainer`.
 """
 
+# We use sys.prefix to find executables as that gets modified with
+# virtualenv's activate_this.py, whereas sys.executable doesn't.
+if platform.system() == 'Windows':
+    bindir = os.path.join(sys.prefix, 'Scripts')
+else:
+    bindir = os.path.join(sys.prefix, 'bin')
+
 results = []
 
 
 class Flake8Process(ProcessHandlerMixin):
     def __init__(self, config, *args, **kwargs):
         self.config = config
         kwargs['processOutputLine'] = [self.process_line]
         ProcessHandlerMixin.__init__(self, *args, **kwargs)
@@ -85,33 +93,22 @@ class Flake8Process(ProcessHandlerMixin)
     def run(self, *args, **kwargs):
         # 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)
         ProcessHandlerMixin.run(self, *args, **kwargs)
         signal.signal(signal.SIGINT, orig)
 
 
-def get_flake8_binary():
-    """
-    Returns the path of the first flake8 binary available
-    if not found returns None
-    """
-    try:
-        return which.which('flake8')
-    except which.WhichError:
-        return None
-
-
 def _run_pip(*args):
     """
     Helper function that runs pip with subprocess
     """
     try:
-        subprocess.check_output(['pip'] + list(args),
+        subprocess.check_output([os.path.join(bindir, 'pip')] + list(args),
                                 stderr=subprocess.STDOUT)
         return True
     except subprocess.CalledProcessError as e:
         print(e.output)
         return False
 
 
 def reinstall_flake8():
@@ -138,19 +135,18 @@ def run_process(config, cmd):
 
 def setup(root):
     if not reinstall_flake8():
         print(FLAKE8_INSTALL_ERROR)
         return 1
 
 
 def lint(paths, config, **lintargs):
-    binary = get_flake8_binary()
     cmdargs = [
-        binary,
+        os.path.join(bindir, 'flake8'),
         '--format', '{"path":"%(path)s","lineno":%(row)s,'
                     '"column":%(col)s,"rule":"%(code)s","message":"%(text)s"}',
     ]
 
     # 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

--- a/tools/lint/python/flake8_requirements.txt
+++ b/tools/lint/python/flake8_requirements.txt
@@ -12,8 +12,11 @@ pycodestyle==2.3.1 \
     --hash=sha256:682256a5b318149ca0d2a9185d365d8864a768a28db66a84a2ea946bcc426766
 enum34==1.1.6 \
     --hash=sha256:6bd0f6ad48ec2aa117d3d141940d484deccda84d4fcd884f5c3d93c23ecd8c79 \
     --hash=sha256:644837f692e5f550741432dd3f223bbb9852018674981b1664e5dc339387588a \
     --hash=sha256:8ad8c4783bf61ded74527bffb48ed9b54166685e4230386a9ed9b1279e2df5b1 \
     --hash=sha256:2d81cbbe0e73112bdfe6ef8576f2238f2ba27dd0d55752a776c41d38b7da2850
 configparser==3.5.0 \
     --hash=sha256:5308b47021bc2340965c371f0f058cc6971a04502638d4244225c49d80db273a
+setuptools==38.5.1 \
+    --hash=sha256:7ffe771abfae419fd104f93400b61c935b5af10bfe4dfeec7a1bd495694eea35 \
+    --hash=sha256:6425484c08e99a98a42209c25c3d325f749230b55284d66192784f941a7e6628