Why am I getting a certificate validation error for what seems to be a valid certificate?
The "bad certificate" error means that your server is expecting your client to authenticate with its own certificate, but when calling requests.get you're not providing one. You want something like:
>>> requests.get(... 'https://docker.local:2376',... cert=['/home/buzzword/.docker/cert.pem', '/home/buzzword/.docker/key.pem']... )(assuming that you have cert.pem and key.pem in your ~/.dockerdirectory)