In 1990, Hunt portrayed Carol Anne Smithson in Grand. She refused to become a cast member of Saturday Night Live because the series’ producers generally frowned on her preferred improvisational style. In 1992, she was offered the part of B. J. Poteet, a replacement for Julia Duffy, on Designing Women.^[7] Instead, she chose to co-star in Davis Rules.

In 1993, Hunt teamed with good friend David Letterman to produce The Building. The series was also filmed live; mistakes, accidents, and forgotten lines were often left in the aired episode.^{[citation needed]} In 1995, Hunt and Letterman reteamed for The Bonnie Hunt Show (later retitled Bonnie), which featured many of the same cast members as The Building and the same loose style. The show was praised by critics but was canceled after 11 of the 13 episodes produced were aired. In 2002, Hunt returned to television with Life with Bonnie. Her role on the series earned her a 2004 Emmy nomination (which was her first). Despite fair ratings, the series was canceled in its second season. Hunt announced on Live with Regis and Kelly that ABC had offered her another sitcom, in which she would have portrayed a divorced detective. This pilot titled Let Go (also known as Crimes and Dating) was not picked up for the fall 2006 schedule.

She directed, co-wrote, and co-starred in Return to Me. It was filmed in her Chicago neighborhood and included bit parts for a number of her relatives. The film, which received a positive reception from critics,^[8] was largely influenced by Hunt’s blue-collar Catholic upbringing in Chicago.^[9]

Hunt portrayed Alice Newton in Beethoven and Beethoven’s 2nd, Sarah Whittle/Madam Serena in Jumanji, and Kate Baker in Cheaper by the Dozen and Cheaper by the Dozen 2. She portrayed the sister of Renée Zellweger’s character in Jerry Maguire and Jan Edgecomb in The Green Mile. She portrayed Grace Bellamy in Loggerheads. She has provided her voice for a total of eight Pixar films: A Bug’s Life as Rosie, Monsters, Inc. as Ms. Flint, Cars, Cars 2, and Cars 3 as Sally Carrera, Toy Story 3 and Toy Story 4 as Dolly, and Monsters University as Karen Graves. In addition, Hunt voiced Bonnie Hopps in the Walt Disney Animation Studios’ film, Zootopia, which marked her first non-Pixar animated film.