diff --git a/changelogs/fragments/ansible-test-constraints-cryptography.yml b/changelogs/fragments/ansible-test-constraints-cryptography.yml
new file mode 100644
index 00000000000..6304a6ce79e
--- /dev/null
+++ b/changelogs/fragments/ansible-test-constraints-cryptography.yml
@@ -0,0 +1,2 @@
+bugfixes:
+  - ansible-test - ``cryptography`` is now limited to versions prior to 3.2 only when an incompatible OpenSSL version (earlier than 1.1.0) is detected
diff --git a/test/lib/ansible_test/_data/cryptography-constraints.txt b/test/lib/ansible_test/_data/cryptography-constraints.txt
index b057c83f9f2..8e3e99b4ae2 100644
--- a/test/lib/ansible_test/_data/cryptography-constraints.txt
+++ b/test/lib/ansible_test/_data/cryptography-constraints.txt
@@ -1,2 +1,3 @@
+# do not add a cryptography constraint here, see the get_cryptography_requirement function in executor.py for details
 idna < 2.8 ; python_version < '2.7' # idna 2.8+ requires python 2.7+
 cffi != 1.14.4 # Fails on systems with older gcc. Should be fixed in the next release. https://foss.heptapod.net/pypy/cffi/-/issues/480
diff --git a/test/lib/ansible_test/_data/requirements/constraints.txt b/test/lib/ansible_test/_data/requirements/constraints.txt
index 9aa52c81a2a..58044f2cc2d 100644
--- a/test/lib/ansible_test/_data/requirements/constraints.txt
+++ b/test/lib/ansible_test/_data/requirements/constraints.txt
@@ -2,7 +2,7 @@ coverage >= 4.5.1, < 5.0.0 ; python_version <  '3.7' # coverage 4.4 required for
 coverage >= 4.5.2, < 5.0.0 ; python_version == '3.7' # coverage 4.5.2 fixes bugs in support for python 3.7, coverage 5.0+ incompatible
 coverage >= 4.5.4, < 5.0.0 ; python_version >  '3.7' # coverage had a bug in < 4.5.4 that would cause unit tests to hang in Python 3.8, coverage 5.0+ incompatible
 cryptography < 2.2 ; python_version < '2.7' # cryptography 2.2 drops support for python 2.6
-cryptography < 3.2 ; python_version >= '2.7'  # cryptography 3.2 drops support for OpenSSL 1.0.2 which some of our CI hosts (FreeBSD) still use
+# do not add a cryptography constraint here unless it is for python version incompatibility, see the get_cryptography_requirement function in executor.py for details
 deepdiff < 4.0.0 ; python_version < '3' # deepdiff 4.0.0 and later require python 3
 jinja2 < 2.11 ; python_version < '2.7' # jinja2 2.11 and later require python 2.7 or later
 urllib3 < 1.24 ; python_version < '2.7' # urllib3 1.24 and later require python 2.7 or later
diff --git a/test/lib/ansible_test/_data/sslcheck.py b/test/lib/ansible_test/_data/sslcheck.py
new file mode 100755
index 00000000000..37b8227936d
--- /dev/null
+++ b/test/lib/ansible_test/_data/sslcheck.py
@@ -0,0 +1,24 @@
+#!/usr/bin/env python
+"""Show openssl version."""
+from __future__ import (absolute_import, division, print_function)
+__metaclass__ = type
+
+import json
+
+# noinspection PyBroadException
+try:
+    from ssl import OPENSSL_VERSION_INFO
+    VERSION = list(OPENSSL_VERSION_INFO[:3])
+except Exception:  # pylint: disable=broad-except
+    VERSION = None
+
+
+def main():
+    """Main program entry point."""
+    print(json.dumps(dict(
+        version=VERSION,
+    )))
+
+
+if __name__ == '__main__':
+    main()
diff --git a/test/lib/ansible_test/_internal/executor.py b/test/lib/ansible_test/_internal/executor.py
index 43fa0d82bca..d127e9cda7a 100644
--- a/test/lib/ansible_test/_internal/executor.py
+++ b/test/lib/ansible_test/_internal/executor.py
@@ -68,6 +68,7 @@ from .util import (
     open_zipfile,
     SUPPORTED_PYTHON_VERSIONS,
     str_to_version,
+    version_to_str,
 )
 
 from .util_common import (
@@ -185,6 +186,42 @@ def create_shell_command(command):
     return cmd
 
 
+def get_openssl_version(args, python, python_version):  # type: (EnvironmentConfig, str, str) -> t.Optional[t.Tuple[int, ...]]
+    """Return the openssl version."""
+    if not python_version.startswith('2.'):
+        # OpenSSL version checking only works on Python 3.x.
+        # This should be the most accurate, since it is the Python we will be using.
+        version = json.loads(run_command(args, [python, os.path.join(ANSIBLE_TEST_DATA_ROOT, 'sslcheck.py')], capture=True, always=True)[0])['version']
+
+        if version:
+            display.info('Detected OpenSSL version %s under Python %s.' % (version_to_str(version), python_version), verbosity=1)
+
+            return tuple(version)
+
+    # Fall back to detecting the OpenSSL version from the CLI.
+    # This should provide an adequate solution on Python 2.x.
+    openssl_path = find_executable('openssl', required=False)
+
+    if openssl_path:
+        try:
+            result = raw_command([openssl_path, 'version'], capture=True)[0]
+        except SubprocessError:
+            result = ''
+
+        match = re.search(r'^OpenSSL (?P<version>[0-9]+\.[0-9]+\.[0-9]+)', result)
+
+        if match:
+            version = str_to_version(match.group('version'))
+
+            display.info('Detected OpenSSL version %s using the openssl CLI.' % version_to_str(version), verbosity=1)
+
+            return version
+
+    display.info('Unable to detect OpenSSL version.', verbosity=1)
+
+    return None
+
+
 def get_setuptools_version(args, python):  # type: (EnvironmentConfig, str) -> t.Tuple[int]
     """Return the setuptools version for the given python."""
     try:
@@ -199,16 +236,21 @@ def get_setuptools_version(args, python):  # type: (EnvironmentConfig, str) -> t
 def get_cryptography_requirement(args, python_version):  # type: (EnvironmentConfig, str) -> str
     """
     Return the correct cryptography requirement for the given python version.
-    The version of cryptograpy installed depends on the python version and setuptools version.
+    The version of cryptography installed depends on the python version, setuptools version and openssl version.
     """
     python = find_python(python_version)
     setuptools_version = get_setuptools_version(args, python)
+    openssl_version = get_openssl_version(args, python, python_version)
 
     if setuptools_version >= (18, 5):
         if python_version == '2.6':
             # cryptography 2.2+ requires python 2.7+
             # see https://github.com/pyca/cryptography/blob/master/CHANGELOG.rst#22---2018-03-19
             cryptography = 'cryptography < 2.2'
+        elif openssl_version and openssl_version < (1, 1, 0):
+            # cryptography 3.2 requires openssl 1.1.x or later
+            # see https://cryptography.io/en/latest/changelog.html#v3-2
+            cryptography = 'cryptography < 3.2'
         else:
             cryptography = 'cryptography'
     else:
diff --git a/test/lib/ansible_test/_internal/util.py b/test/lib/ansible_test/_internal/util.py
index 141048b17c2..2480a8a6682 100644
--- a/test/lib/ansible_test/_internal/util.py
+++ b/test/lib/ansible_test/_internal/util.py
@@ -771,12 +771,12 @@ def paths_to_dirs(paths):  # type: (t.List[str]) -> t.List[str]
     return sorted(dir_names)
 
 
-def str_to_version(version):  # type: (str) -> t.Tuple[int]
+def str_to_version(version):  # type: (str) -> t.Tuple[int, ...]
     """Return a version tuple from a version string."""
     return tuple(int(n) for n in version.split('.'))
 
 
-def version_to_str(version):  # type: (t.Tuple[int]) -> str
+def version_to_str(version):  # type: (t.Tuple[int, ...]) -> str
     """Return a version string from a version tuple."""
     return '.'.join(str(n) for n in version)