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Peter Weller made his Broadway debut as David in the New York Shakespeare Festival's Tony Award winning production of David Rabe's Sticks and Bones, (a role he re-created for the London premiere). He also starred as Billy Wilson in David Rabe's Streamers, directed by Mike Nichols at Lincoln Center. Weller originated the role of Nick in David Mamet's, The Woods in Chicago at Mamet's St. Nicholas Theater. Weller reprised the role under Mamet's direction at the Second Stage in New York. Also for Second Stage, at the New York Shakespeare Festival, he starred opposite Diane Wiest in Lanford Wilson's rework of Serenading Louie. Other New York performances include: James Purdy's Daddy Wolf at the Ensemble Studio Theater; Tom Babe's Rebel Women at the NY Shakespeare festival; and the ubiquitous Cliff in the original production of William Mastrosimones's The Woolgatherer at Circle Repertory. He also starred on stage in two Tennessee Williams works with Christine Lahti in Cat on a Hot Tin Roof and with Shirley Knight in A Streetcar Named Desire.

On television, Weller starred with Molly Ringwald, Elizabeth McGovern, Beau Bridges, Melanie Griffith and James Woods in David Brown's much heralded HBO special Tales of Seduction – three great American short stories adapted for the screen; Weller was featured in the Dorothy Parker segment of the trilogy, Dusk Before Fireworks, directed by Ken Russell.

Weller's film starring credits include: Richard Lester's Butch and Sundance: The Early Years, Sidney Lumet's Just Tell Me What You Want, Alan Parker's Shoot The Moon with Diane Keaton and Albert Finney, George Cosmatos' Of Unknown Origin (for which Weller won the Best Actor award from the International Film Festival of Paris), the title role in the now classic Adventures of Buckaroo Banzai, Michael Apted's Firstborn, Abel Ferrara's film of Elmore Leonard's Cat Chaser, Shakedown with Sam Elliot, 50/50 with Robert Hayes, directed by Charles Martin Smith. Weller created the amazing metal man in the original Robocop.

Weller was nominated for the Canadian Oscar for his performance as William Lee in David Cronenberg's film of the William Burrough's literary classic Naked Lunch, also starring Judy Davis. He also starred in the Addis/Wechsler production of Michael Tolkin's The New Age, again opposite Judy Davis, and executive produced by Oliver Stone. Weller starred in Decoy, Screamers, Woody Allen's Mighty Aphrodite, Par-Dela Les Nuages directed by Michelangelo Antonioni and Top of the World with Dennis Hopper.