OrcaBot: There's a lot there! Ambitious project. Cute name, who doesn't love orcas? I don't see anything screamingly bad, of the variety that would inspire me to write essays about random people's code.
Some thoughts: The line between dev mode and production is a bit thin and lightly enforced. Given the overall security approach, you could firm that up. The within-VM shared workspace undermines the isolated PTYs. If your rate-limiting middleware fails, you allow all requests through. `SECRETS_ENCRYPTION_KEY` is the one ring and it doesn't have any versioning or rotation mechanisms.
In general it seems like a good approach! But there are spots where one thing being misconfigured could blow the entire system open. I suggest taking a pass through it with that in mind. Good luck.