diff --git a/certbot/display/util.py b/certbot/display/util.py
index 7e797e71a..5b01dd8d4 100644
--- a/certbot/display/util.py
+++ b/certbot/display/util.py
@@ -69,6 +69,8 @@ def input_with_timeout(prompt=None, timeout=36000.0):
     :raises errors.Error if no answer is given before the timeout
 
     """
+    # use of sys.stdin and sys.stdout to mimic six.moves.input based on
+    # https://github.com/python/cpython/blob/baf7bb30a02aabde260143136bdf5b3738a1d409/Lib/getpass.py#L129
     if prompt:
         sys.stdout.write(prompt)
         sys.stdout.flush()
@@ -79,7 +81,10 @@ def input_with_timeout(prompt=None, timeout=36000.0):
         raise errors.Error(
             "Timed out waiting for answer to prompt '{0}'".format(prompt))
 
-    return rlist[0].readline().rstrip('\n')
+    line = rlist[0].readline()
+    if not line:
+        raise EOFError
+    return line.rstrip('\n')
 
 
 @zope.interface.implementer(interfaces.IDisplay)
diff --git a/certbot/tests/display/util_test.py b/certbot/tests/display/util_test.py
index a872917ec..1dfc21c30 100644
--- a/certbot/tests/display/util_test.py
+++ b/certbot/tests/display/util_test.py
@@ -2,6 +2,7 @@
 import inspect
 import os
 import socket
+import tempfile
 import unittest
 
 import six
@@ -25,15 +26,17 @@ class InputWithTimeoutTest(unittest.TestCase):
         from certbot.display.util import input_with_timeout
         return input_with_timeout(*args, **kwargs)
 
-    def setUp(self):
-        self.expected_msg = "foo bar"
-        self.stdin = six.StringIO(self.expected_msg + "\n")
+    def test_eof(self):
+        with tempfile.TemporaryFile("r+") as f:
+            with mock.patch("certbot.display.util.sys.stdin", new=f):
+                self.assertRaises(EOFError, self._call)
 
     def test_input(self, prompt=None):
+        expected = "foo bar"
+        stdin = six.StringIO(expected + "\n")
         with mock.patch("certbot.display.util.select.select") as mock_select:
-            mock_select.return_value = ([self.stdin], [], [],)
-            self.assertEqual(display_util.input_with_timeout(prompt),
-                             self.expected_msg)
+            mock_select.return_value = ([stdin], [], [],)
+            self.assertEqual(self._call(prompt), expected)
 
     @mock.patch("certbot.display.util.sys.stdout")
     def test_input_with_prompt(self, mock_stdout):