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Smith began acting in 1982 after graduating from drama school. She moved to New York City in 1984, where she appeared in the Broadway production of Tom Stoppard's The Real Thing. She made her film debut in 1985's Heaven Help Us, followed by roles in The Legend of Billie Jean and Maximum Overdrive. She moved to Los Angeles in 1986 and took a recurring role in the television series Brothers.

In 1987, Smith auditioned for the Simpsons shorts on The Tracey Ullman Show. Smith intended to audition for the role of Bart Simpson, but the casting director felt her voice was too high, and she was cast as Bart's sister Lisa. In 1989, the shorts were spun off into their own half-hour show, The Simpsons. For her work on The Simpsons, Smith received a Primetime Emmy Award for Outstanding Voice-Over Performance in 1992.

Alongside The Simpsons, Smith appeared in the sitcom Herman's Head as Louise, and had recurring appearances as Marlene on Dharma & Greg and as Penny in two episodes of Dead Like Me. She has appeared in several films, including City Slickers, Just Write, Toys, and As Good as It Gets. In 2004, Smith performed an off-Broadway one-woman show entitled More at the Union Square Theatre in New York City. Aside from The Simpsons, Smith has recorded few voice-over parts, only commercials and the film We're Back! A Dinosaur's Story. Smith starred in and served as executive producer for the independent romantic comedy Waiting For Ophelia, which had its world premiere at the Phoenix Film Festival in April 2009.