Born in Plainsfield, New Jersey, Rule was educated in California and England. In 1956, she moved to Vancouver, British Columbia, where she became affiliated with the University of British Columbia, working there until 1974 as a periodic and visiting lecturer in English and Creative writing.

Here also, she met Helen Sonthoff, her partner and helpmate for over 40 years, with whom in 1956 she moved to live together, sharing home on Galiano Island, until Sonthoff death in 1999.

Her book Desert of the Heart was made into the lesbian film classic Desert Hearts (1985). Anti-censorship activist, novelist, and journalist, she is the subject of the film Fiction and Other Truths: A Film About Jane Rule, by Lynne Fernie and Aerlyn Weissman.