1) Testing a Dockerfile, then scp'd it to the server, doesn't guarantee that it will build successfully on the server. However if you build successfully an image and push it to a repository - it will definitely work. Based on this, you can decide which one works for your setup. If you are on a production setup, I would say that you should use tested images, instead of hoping that the Dockerfile will build correctly.

3) As far as I understand your problem is that both containers would be running their own nginx, and would have to take port 80 for example. If this is what you mean, you could just EXPOSE port 80 from within the container, and it will automatically be mapped to a random port like 43152. Both containers would be mapped to different random ports (for example 43152 and 43153). You could then install Hipache and route different domain names/sites to different containers, essentially having Hipache proxy in front your Docker containers setup.

EDIT: There is also a project called Shipyard, which is Docker management... what I described above is called "Applications" inside Shipyard.

[0] https://github.com/shipyard/shipyard [1] https://github.com/dotcloud/hipache