Following a series of television roles, Balk made her feature film debut as Dorothy Gale in Return to Oz (1985), for which she was nominated for a Young Artist Award for Best Starring Performance.

Her career progressed with parts in films such as Valmont (1989) and Gas Food Lodging (1992), the latter earning her an Independent Spirit Award for Best Female Lead.

After roles in Imaginary Crimes (1994) and Things to Do in Denver When You're Dead (1995), Balk received acclaim and a cult following for her portrayal of Nancy Downs in The Craft (1996), which earned her an MTV Movie Award.

She played the recurring role of Ginger on Showtime's Ray Donovan in 2015, and starred as Lizzie Thomas in the Amazon Prime series Paradise City in 2021.

In 1998, she played a neo-Nazi opposite Edward Norton in American History X, and was featured in The Waterboy, alongside Adam Sandler.

She has also done voice work for animated films, TV shows and video games, including Justice League, Family Guy, Grand Theft Auto: Vice City and Lords of EverQuest.

On August 4, 2012, she participated in the group show 'MiXTAPE', with other notable artists Mark Ryden, Camille Rose Garcia, Jessicka Addams, and Marion Peck.

[12][13][14] In 2017, the emo puppet band Fragile Rock performed a song titled "Fairuza Balk" on their NPR Tiny Desk Concert.