diff --git a/changelog/5059.feature.rst b/changelog/5059.feature.rst
new file mode 100644
index 000000000..4d5d14061
--- /dev/null
+++ b/changelog/5059.feature.rst
@@ -0,0 +1 @@
+Standard input (stdin) can be given to pytester's ``Testdir.run()`` and ``Testdir.popen()``.
diff --git a/changelog/5059.trivial.rst b/changelog/5059.trivial.rst
new file mode 100644
index 000000000..bd8035669
--- /dev/null
+++ b/changelog/5059.trivial.rst
@@ -0,0 +1 @@
+pytester's ``Testdir.popen()`` uses ``stdout`` and ``stderr`` via keyword arguments with defaults now (``subprocess.PIPE``).
diff --git a/src/_pytest/pytester.py b/src/_pytest/pytester.py
index d474df4b9..6dc9031df 100644
--- a/src/_pytest/pytester.py
+++ b/src/_pytest/pytester.py
@@ -473,6 +473,8 @@ class Testdir(object):
 
     """
 
+    CLOSE_STDIN = object
+
     class TimeoutExpired(Exception):
         pass
 
@@ -1032,7 +1034,14 @@ class Testdir(object):
             if colitem.name == name:
                 return colitem
 
-    def popen(self, cmdargs, stdout, stderr, **kw):
+    def popen(
+        self,
+        cmdargs,
+        stdout=subprocess.PIPE,
+        stderr=subprocess.PIPE,
+        stdin=CLOSE_STDIN,
+        **kw
+    ):
         """Invoke subprocess.Popen.
 
         This calls subprocess.Popen making sure the current working directory
@@ -1050,10 +1059,18 @@ class Testdir(object):
         env["USERPROFILE"] = env["HOME"]
         kw["env"] = env
 
-        popen = subprocess.Popen(
-            cmdargs, stdin=subprocess.PIPE, stdout=stdout, stderr=stderr, **kw
-        )
-        popen.stdin.close()
+        if stdin is Testdir.CLOSE_STDIN:
+            kw["stdin"] = subprocess.PIPE
+        elif isinstance(stdin, bytes):
+            kw["stdin"] = subprocess.PIPE
+        else:
+            kw["stdin"] = stdin
+
+        popen = subprocess.Popen(cmdargs, stdout=stdout, stderr=stderr, **kw)
+        if stdin is Testdir.CLOSE_STDIN:
+            popen.stdin.close()
+        elif isinstance(stdin, bytes):
+            popen.stdin.write(stdin)
 
         return popen
 
@@ -1065,6 +1082,10 @@ class Testdir(object):
         :param args: the sequence of arguments to pass to `subprocess.Popen()`
         :param timeout: the period in seconds after which to timeout and raise
             :py:class:`Testdir.TimeoutExpired`
+        :param stdin: optional standard input.  Bytes are being send, closing
+            the pipe, otherwise it is passed through to ``popen``.
+            Defaults to ``CLOSE_STDIN``, which translates to using a pipe
+            (``subprocess.PIPE``) that gets closed.
 
         Returns a :py:class:`RunResult`.
 
@@ -1072,6 +1093,7 @@ class Testdir(object):
         __tracebackhide__ = True
 
         timeout = kwargs.pop("timeout", None)
+        stdin = kwargs.pop("stdin", Testdir.CLOSE_STDIN)
         raise_on_kwargs(kwargs)
 
         cmdargs = [
@@ -1086,8 +1108,14 @@ class Testdir(object):
         try:
             now = time.time()
             popen = self.popen(
-                cmdargs, stdout=f1, stderr=f2, close_fds=(sys.platform != "win32")
+                cmdargs,
+                stdin=stdin,
+                stdout=f1,
+                stderr=f2,
+                close_fds=(sys.platform != "win32"),
             )
+            if isinstance(stdin, bytes):
+                popen.stdin.close()
 
             def handle_timeout():
                 __tracebackhide__ = True
diff --git a/testing/test_pytester.py b/testing/test_pytester.py
index 2e4877463..b76d413b7 100644
--- a/testing/test_pytester.py
+++ b/testing/test_pytester.py
@@ -4,6 +4,7 @@ from __future__ import division
 from __future__ import print_function
 
 import os
+import subprocess
 import sys
 import time
 
@@ -482,3 +483,79 @@ def test_pytester_addopts(request, monkeypatch):
         testdir.finalize()
 
     assert os.environ["PYTEST_ADDOPTS"] == "--orig-unused"
+
+
+def test_run_stdin(testdir):
+    with pytest.raises(testdir.TimeoutExpired):
+        testdir.run(
+            sys.executable,
+            "-c",
+            "import sys, time; time.sleep(1); print(sys.stdin.read())",
+            stdin=subprocess.PIPE,
+            timeout=0.1,
+        )
+
+    with pytest.raises(testdir.TimeoutExpired):
+        result = testdir.run(
+            sys.executable,
+            "-c",
+            "import sys, time; time.sleep(1); print(sys.stdin.read())",
+            stdin=b"input\n2ndline",
+            timeout=0.1,
+        )
+
+    result = testdir.run(
+        sys.executable,
+        "-c",
+        "import sys; print(sys.stdin.read())",
+        stdin=b"input\n2ndline",
+    )
+    assert result.stdout.lines == ["input", "2ndline"]
+    assert result.stderr.str() == ""
+    assert result.ret == 0
+
+
+def test_popen_stdin_pipe(testdir):
+    proc = testdir.popen(
+        [sys.executable, "-c", "import sys; print(sys.stdin.read())"],
+        stdout=subprocess.PIPE,
+        stderr=subprocess.PIPE,
+        stdin=subprocess.PIPE,
+    )
+    stdin = b"input\n2ndline"
+    stdout, stderr = proc.communicate(input=stdin)
+    assert stdout.decode("utf8").splitlines() == ["input", "2ndline"]
+    assert stderr == b""
+    assert proc.returncode == 0
+
+
+def test_popen_stdin_bytes(testdir):
+    proc = testdir.popen(
+        [sys.executable, "-c", "import sys; print(sys.stdin.read())"],
+        stdout=subprocess.PIPE,
+        stderr=subprocess.PIPE,
+        stdin=b"input\n2ndline",
+    )
+    stdout, stderr = proc.communicate()
+    assert stdout.decode("utf8").splitlines() == ["input", "2ndline"]
+    assert stderr == b""
+    assert proc.returncode == 0
+
+
+def test_popen_default_stdin_stderr_and_stdin_None(testdir):
+    # stdout, stderr default to pipes,
+    # stdin can be None to not close the pipe, avoiding
+    # "ValueError: flush of closed file" with `communicate()`.
+    p1 = testdir.makepyfile(
+        """
+        import sys
+        print(sys.stdin.read())  # empty
+        print('stdout')
+        sys.stderr.write('stderr')
+        """
+    )
+    proc = testdir.popen([sys.executable, str(p1)], stdin=None)
+    stdout, stderr = proc.communicate(b"ignored")
+    assert stdout.splitlines() == [b"", b"stdout"]
+    assert stderr.splitlines() == [b"stderr"]
+    assert proc.returncode == 0