@bur There's no reason this shouldn't be possible - I saw Drastic DS emulator on Android has dual screen support - so at least on Android it's possible with Raspberry Pi. I'm waiting on a HDMI 3.5 inch screen so I can test it with my 5inch Waveshare screen, and I'll report back if I have any success.
As for doing it in Raspbian, I sure hope that would work but no idea at this point.