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She initially appeared in a 1989 episode of the hit sitcom Cheers, playing a character named Emily. She also starred in several episodes of the show Mad About You(1993) as Ursula before auditioning and earning the role of Phoebe on Friends; her character on Mad About You was written into the Friends storyline as Phoebe's twin. In the late 1990s, she starred in the cult comedy film Romy and Michele's High School Reunion (1997) and followed it with an acclaimed performance in the comedy/drama The Opposite of Sex (1998), which won her the New York Film Critics Circle Award for Best Supporting Actress and a nomination for the Independent Spirit Award for Best Supporting Female. She created, produced, wrote, and starred in the HBO mockumentary series The Comeback, which initially lasted for one season in 2005 but was revived for a critically acclaimed second and final season in 2014. She was nominated for the Primetime Emmy Award for Outstanding Lead Actress in a Comedy Series for both seasons.

In 2007, she received praise for her starring role in the film Kabluey and appeared in P.S. I Love You. She produced and starred in the Showtime program Web Therapy (2011–2015), which was nominated for a Primetime Emmy Award. She is a producer on the TLC/NBC reality program Who Do You Think You Are, which has been nominated for a Primetime Emmy Award five times. She played Honey the Dog on the FOX animated series HouseBroken.

She has also had roles in Analyze This (1999) and its sequel, Analyze That (2002), Dr. Dolittle 2 (2001), Bandslam (2008), Hotel for Dogs (2009), Easy A (2010), Neighbors (2014) and its sequel Neighbors 2: Sorority Rising (2016), The Girl on the Train (2016), The Boss Baby (2017), Long Shot (2019), and Booksmart (2019).