> A separate machine/VM is better from an availability perspective.
How so? A separate machine is one more thing that can fail and since it isn't web facing it won't help with availability if the other one fails. And if it is a VM they will both go down if the underlying hardware fails.
Its true that a separate machine is one more thing that can fail, but if its purpose is so different, as with the "active CMS" - "static hosting service", then it becomes easier to create a replacement.
E.g. the frontend can be replicated (if needed), S3 can be used, while the backend CMS remains intact. Or the backend CMS can be implemented in a HA setup and the static hosting in the cloud.
How so? A separate machine is one more thing that can fail and since it isn't web facing it won't help with availability if the other one fails. And if it is a VM they will both go down if the underlying hardware fails.