Hunt began working in the 1970s as a child actress. Her early roles included an appearance as Murray Slaughter's daughter on The Mary Tyler Moore Show, alongside Lindsay Wagner in an episode of The Bionic Woman, and a regular role in the television series The Swiss Family Robinson. She appeared as a marijuana-smoking classmate on an episode of The Facts of Life. She also appeared as a young woman who, while on PCP, jumps out of a second-story window in a 1982 after school special called Desperate Lives (a scene which she mocked during a Saturday Night Live monologue in 1994). In the mid-1980s, she had a recurring role on St. Elsewhere as Clancy Williams, girlfriend of Dr. Jack "Boomer" Morrison. She remains best known for one of her earliest roles as Jennie in Bill: On His Own, costarring Mickey Rooney.

In the 1990s, after the lead female role in the short-lived My Life and Times, Hunt became well-known to television audiences in Mad About You, winning Emmy Awards for her performance in 1996, 1997, 1998, and 1999. Hunt has also had a successful film career, with roles in movies such as Cast Away and the 1996 blockbuster Twister. In 1998 Hunt won an Academy Award for Best Actress for her portrayal of Carol Connelly, a waitress and single mother who finds herself falling in love with Melvin Udall, an obsessive-compulsive romance novelist played by Jack Nicholson in the movie As Good as It Gets. After winning the Academy Award she took several years off from movie work to play Viola in Shakespeare's Twelfth Night at Lincoln Center in New York City.

In 2000, Hunt returned to the screen in four films: Dr. T & the Women with Richard Gere, Pay It Forward with Kevin Spacey and Haley Joel Osment, What Women Want with Mel Gibson, and Cast Away with Tom Hanks. In 2003, she returned to Broadway in Yasmina Reza's Life x 3. Hunt was also a final candidate for the role of "Clarice Starling" in Hannibal, after Jodie Foster decided not to reprise her Oscar winning role from The Silence of the Lambs. However, Hunt lost the role to Julianne Moore at the last minute. In 2006, Hunt appeared in a small role in the film Bobby. Hunt is a director, having helmed several episodes of Mad About You, including the series finale. Her big-screen directorial debut came with the film Then She Found Me, in which she also starred. She currently owns a production company with Connie Tavel, Hunt/Tavel Productions under Sony Pictures Entertainment.

• Every Day (2009) (post-production) .... Jeannie
  
• Then She Found Me (2007) .... April Epner
• Bobby (2006) .... Samantha
• Empire Falls (2005) (TV) .... Janine Roby
• A Good Woman (2004) .... Mrs. Erlynne
  ... aka Seduttrici, Le (Italy)
• The Curse of the Jade Scorpion (2001) .... Betty Ann Fitzgerald
  ... aka Im Bann des Jade Skorpions (Germany)
• One Night at McCool's (2001) (scenes deleted) .... Truck Driver
• What Women Want (2000) .... Darcy McGuire
• Cast Away (2000) .... Kelly Frears
• Pay It Forward (2000) .... Arlene McKinney
• Dr T and the Women (2000) .... Bree
  ... aka Dr. T and the Women (Germany) (USA: alternative spelling)
  
  
• "Mad About You" .... Jamie Stemple Buchman (161 episodes, 1992-1999)
       - The Final Frontier (1999) TV episode .... Jamie Stemple Buchman
       - The Dirty Little Secret (1999) TV episode .... Jamie Stemple Buchman
       - Paved with Good Intentions (1999) TV episode .... Jamie Stemple Buchman
       - Stealing Burt's Car (1999) TV episode .... Jamie Stemple Buchman
       - Separate Beds (1999) TV episode .... Jamie Stemple Buchman
        (156 more)
• Twelfth Night, or What You Will (1998) (TV) .... Viola
• "The Simpsons" .... Renee (1 episode, 1998)
       - Dumbbell Indemnity (1998) TV episode (voice) .... Renee
• As Good as It Gets (1997) .... Carol Connelly
• Twister (1996) .... Dr. Jo Harding
• Kiss of Death (1995/I) .... Bev Kilmartin
• "Friends" .... Jamie Buchman (1 episode, 1995)
       - The One with Two Parts: Part 1 (1995) TV episode .... Jamie Buchman
• In the Company of Darkness (1993) (TV) .... Gina Pulasky
• Sexual Healing (1993) .... Rene
• Trancers III (1992) (V) .... Lena
  ... aka Death Lives
  ... aka Future Cop III
• Mr. Saturday Night (1992) .... Annie Wells