Morrisseau was a self-taught artist. He developed his own techniques and artistic vocabulary that captured ancient legends and images that came to him in visions or dreams. He was originally criticized by the native community because his images disclosed traditional spiritual knowledge. Initially he painted on any material that he could find, especially birchbark, and also moose hide. Dewdney encouraged him to use earth-tone colors and traditional material, which he thought were appropriate to Morrisseau's native style.

Morrisseau, who was bisexual, also produced erotic works featuring sexuality between male figures and between male and female figures. Most of these works are now held in private collections. Other works explored Indigenous conceptions of gender fluidity, such as his massive work Androgyny (1983), which was formerly exhibited at Rideau Hall.