Hunter earned a degree in drama from Carnegie Mellon University, after which she moved to New York City. When she first moved to Los Angeles she shared a house with a group of people which included actress Frances McDormand and director Sam Raimi as well as future collaborators Joel and Ethan Coen. For many years she was in a relationship with actor Arliss Howard. She was married to cinematographer Janusz Kaminski from May 20, 1995 until their divorce on December 21, 2001. Since 2001, she has been in a relationship with British actor Gordon MacDonald, with whom she co-starred in Marina Carr's By the Bog of Cats in a 2001 run at the San Jose Repertory Theater, and later in a 2004 West End production. In January 2006, Hunter's publicist announced that the couple had welcomed twins; Entertainment Weekly later reported that the twins were boys.