She was born in Winona, Minnesota, and apparently she was named after her birthplace. Notable family friends included her godfather Timothy Leary and Beat poet Allen Ginsberg. About ten years later, the family moved to Petaluma, Sonoma County, California. Winona attended the local American Conservatory Theater where she started taking acting lessons.
She got into legal trouble in December 2001 when she was caught after a $5,500 shoplifting spree at Saks Fifth Avenue department store in Beverly Hills, California. In 2002 she was sentenced to 480 hours of community service.
Her film debut was in Lucas, directed by David Seltzer and first released on March 28, 1986. The film was a tragicomedy intended towards a teen audience. The title character was Lucas (Corey Haim), a somewhat nerdy high school student who finds himself an often victim of bullying. Cappie (Charlie Sheen), a fellow student and American football athlete tends to places him under his protection. Both are soon acquainted to new student Maggie (Kerri Green) and seem to fall for her. But she is only interested in Cappie. Lucas then attempts to gain acceptance by entering the football team himself. His efforts attract the attention of Winona's character Rina. The rest of the film concetrates on Lucas' subsequent experiences, resulting in his gradual maturing process. The film was moderately successful and both Corey Haim and Kerri Green were nomitated for a Young Artist Award in 1987. Winona first gained public attention through her performance.
She made her second film appearance in Square Dance, written by Alan Hines, directed by Daniel Petrie and first released in March, 1987. Winona starred as Gemma, a 13 year-old country girl who lives with her Grandpa Dillard (Jason Robards). At some point, Gemma is visited by her mother with an offer to come stay with her in the city. Her mother is now married and can provide for her. Gemma accepts and soon finds herself in a new environment. She is acquainted and grows close to the mentaly retarded Rory (Rob Lowe). The rest of the film focuses in a series of bitter-sweet experiences that eventualy return Gemma to the country. The film was not commercially successful but Rob Lowe was nominated for a Golden Globe Award.
Her film credits include Beetlejuice (1988), The Age of Innocence and Little Women (which scored her Oscar nominations in 1994 and '95), Mermaids, Heathers, Bram Stoker's Dracula, The Crucible, Alien: Resurrection and Mr Deeds(2002). She also executive produced and starred in Girl, Interrupted.