How can a single nginx virtual server deal with both port 80 and 443?

Yes, of course.

server {
  listen 80;
  listen 443 ssl;
  # force https-redirects
  if ($scheme = http) {
    return 301 https://$server_name$request_uri;
  }
}

Here is my post, name “Nginx Configuration for HTTPS” which contains more info.