Mutual TLS Authentication - SSLV3_ALERT_UNSUPPORTED_CERTIFICATE

I currently am trying to implement mutual TLS authentication between a client and a server. I'm running into an SSL error and it is not very descriptive. StackOverflow also does not have many questions related to it since most of the time it is a one-way TLS on the internet. However, from what I've seen, this error occurs because something is wrong with the client certificate, so below I have attached information relevant to that. If that is not the case, please let me know.

Generating Client Cert

My client's cnf(foo.config) looks like(with replacing all the sensitive information):

[ req ]
default_bits = 2048
default_md = sha256
prompt = no
req_extensions = req_ext
distinguished_name = dn
encrypt_key = no

[ dn ]
O=Bar
OU=User
CN=myuser@foo.com

[ req_ext ]
subjectAltName = email:myuser@foo.com
nsCertType = client, email, objsign
keyUsage = nonRepudiation, digitalSignature, keyEncipherment

I pass in this config file using openssl to create a csr:

openssl req -new -sha256 -key foo.key -out foo.csr -config foo.config

And then I send it to an infrastructure management API internally to sign the x509 certificate. I save the client certificate as foo.cert(it contains the trust chain up to the CA).

How my client sends the cert

When I send a urllib open request to my server, I send the ssl context with my HTTPSConnection:

... # Inside some handler code
context = ssl.create_default_context(purpose=ssl.Purpose.SERVER_AUTH,
            cafile=ROOT_CA)
context.load_cert_chain(certfile=CERT_DEST, keyfile=KEY_DEST)
context.verify_mode = ssl.CERT_REQUIRED
context.check_hostname = True
return http.client.HTTPSConnection(host, context=context)

How my flask server sets up

When my testing flask server takes in the ssl context like so:

executor = Flask(__name__)
context = ssl.create_default_context(purpose=ssl.Purpose.CLIENT_AUTH, cafile=TEST_CA_CERT)
context.load_cert_chain(certfile=TEST_CERT, keyfile=TEST_KEY)
context.verify_mode = ssl.CERT_REQUIRED
context.check_hostname = False
executor.run(host=host, port=port, ssl_context=context)

It sets up its own certificates an key files. It also sets up client authentication requests.

Full error traceback

Upon runtime, during a call, I get this traceback(replacing all sensitive information):

Traceback (most recent call last):
  File "/auto/foo/python3-rhel6/lib/python3.6/urllib/request.py", line 1318, in do_open
    encode_chunked=req.has_header('Transfer-encoding'))
  File "/auto/foo/python3-rhel6/lib/python3.6/http/client.py", line 1239, in request
    self._send_request(method, url, body, headers, encode_chunked)
  File "/auto/foo/python3-rhel6/lib/python3.6/http/client.py", line 1285, in _send_request
    self.endheaders(body, encode_chunked=encode_chunked)
  File "/auto/foo/python3-rhel6/lib/python3.6/http/client.py", line 1234, in endheaders
    self._send_output(message_body, encode_chunked=encode_chunked)
  File "/auto/foo/python3-rhel6/lib/python3.6/http/client.py", line 1026, in _send_output
    self.send(msg)
  File "/auto/foo/python3-rhel6/lib/python3.6/http/client.py", line 964, in send
    self.connect()
  File "/auto/foo/python3-rhel6/lib/python3.6/http/client.py", line 1400, in connect
    server_hostname=server_hostname)
  File "/auto/foo/python3-rhel6/lib/python3.6/ssl.py", line 407, in wrap_socket
    _context=self, _session=session)
  File "/auto/foo/python3-rhel6/lib/python3.6/ssl.py", line 814, in __init__
    self.do_handshake()
  File "/auto/foo/python3-rhel6/lib/python3.6/ssl.py", line 1068, in do_handshake
    self._sslobj.do_handshake()
  File "/auto/foo/python3-rhel6/lib/python3.6/ssl.py", line 689, in do_handshake
    self._sslobj.do_handshake()
ssl.SSLError: [SSL: SSLV3_ALERT_UNSUPPORTED_CERTIFICATE] sslv3 alert unsupported certificate (_ssl.c:833)

During handling of the above exception, another exception occurred:

Traceback (most recent call last):
  File "./bar.py", line 375, in <module>
    start(args, overrides, threadlock)
  File "./bar.py", line 332, in start
    approved, alloc_message = Executor.approve(flow.the_portal.inst)
  File "/home/myuser/dev/bar/Executor.py", line 638, in approve
    with opener.open(request, json_request) as response:
  File "/auto/foo/python3-rhel6/lib/python3.6/urllib/request.py", line 526, in open
    response = self._open(req, data)
  File "/auto/foo/python3-rhel6/lib/python3.6/urllib/request.py", line 544, in _open
    '_open', req)
  File "/auto/foo/python3-rhel6/lib/python3.6/urllib/request.py", line 504, in _call_chain
    result = func(*args)
  File "/home/myuser/dev/bar/Auth.py", line 77, in https_open
    return self.do_open(self.getConnection, req)
  File "/auto/foo/python3-rhel6/lib/python3.6/urllib/request.py", line 1320, in do_open
    raise URLError(err)
urllib.error.URLError: <urlopen error [SSL: SSLV3_ALERT_UNSUPPORTED_CERTIFICATE] sslv3 alert unsupported certificate (_ssl.c:833)>

If more information is required, please don't hesitate to let me know. Any help would be appreciated.

EDIT: Here's the certificate (in redacted form):

Certificate:
    Data:
        Version: 3 (0x2)
        Serial Number:
            ...
    Signature Algorithm: sha256WithRSAEncryption
        Issuer: DC=com, DC=foo, CN=Foo Issuing CA - XXX
        Validity
            Not Before: ... 2018 GMT
            Not After : ... GMT
        Subject: O=Bar, OU=User, CN=myuser@foo.com
        Subject Public Key Info:
            Public Key Algorithm: rsaEncryption
                ...
        X509v3 extensions:
            X509v3 Key Usage:
                Key Encipherment, Data Encipherment
            X509v3 Subject Alternative Name:
                email:myuser@foo.com
            X509v3 Subject Key Identifier:
                ...
            X509v3 Authority Key Identifier:
                ...

            X509v3 CRL Distribution Points:

                Full Name:
                    ...
            Authority Information Access:
                CA Issuers - ...
                CA Issuers - ...

            X509v3 Extended Key Usage:
                TLS Web Server Authentication, TLS Web Client Authentication

Verifying this file with my cert bundle says:

openssl verify -CAfile /.../certification_bundle.pem foo.cert
foo.cert: OK

from Mutual TLS Authentication - SSLV3_ALERT_UNSUPPORTED_CERTIFICATE