Hunt was born in Chicago, as one of seven children. For a while, Hunt worked as a cancer nurse at Northwestern Memorial Hospital in Chicago. In the mid 1980s, Hunt cofounded "An Impulsive Thing", a the three woman improvisational comedy troupe, with Holly Wortell and Joan Cusack. The women performed regularly in Chicago. Hunt also performed as a member of the Second City.
Hunt turned down multiple opportunities to become a cast member of Saturday Night Live, because the shows producers generally frown on improvisation on the show.
In 1992, Hunt turned down a higher paying role on Designing Women to costar in Davis Rules with Jonathan Winters and Audrey Meadows. Hunt was also offered Helen Hunt's role on Mad About You, but turned it down as well.
In 1993, Hunt teamed up with David Letterman to produce The Building for CBS. The sitcom was modeled after early 1950s television shows in many ways, including being filmed in front of a studio audience. The show was also essentially filmed "live", meaning mistakes, accidents and forgotten lines often made it into the aired episode. The writing of the show tended to be very loose, which allowed the actors to improvise. Despite being praised by television critics, the show was soon cancelled.
Hunt and Letterman gave it another shot in 1995, with The Bonnie Hunt Show (later retitled just Bonnie), which featured many of the same cast members as The Building and the same loose style. The show was once again praised by critics and soon cancelled. In 2002, Hunt returned to television with Life with Bonnie.
Hunt also frequently appears on the silver screen in major motion pictures, including Monsters, Inc, The Green Mile with Tom Hanks, Random Hearts with Harrison Ford, A Bug's Life, Jerry Maguire with Tom Cruise, Jumanji with Robin Williams, Beethoven and Rain Man.