(I do not have experience with Raspberry Pi)
To answer your question kind of... in pieces:
Raspberry Pi 4 natively uses OpenGL ES 3.1, and natively supports OpenGL 2.2 (allegedly).
Although I have found resources that purport to unlocking the Pi 4 to versions of OpenGL as late as roughly 3.3.
It's not entirely clear what OpenGLs the Videocore VI chip is actually capable of, but it seems people are running Blender 2.79b, and games like Open Arena, just fine.
In terms of [does R. Pi 4 have the power]: yes (Hardware meets spec)
In terms of [does R. Pi 4 have the software]: yes (Hardware meets reqs)
In terms of [does R. Pi 4 have the firmware]: it seems so (soft yes)
In terms of [does R. Pi 4 have the API/Middleware]: it kind of seems so (maybe)
If you're using Blender 2.79b, and the old vanilla engine within it, and you also are not using any advanced shaders or Eevee (UPBGE), then all signs point to a... :
Soft Yes
References...