The sloe-eyed brunette made her onscreen debut in Craig Singer's Animal Room (1996). That same year, she could also be seen in an episode of Law & Order, and went on to play a role in Grind (1996), a crime drama starring Billy Crudup. Before long, Peet landed a small role the Michelle Pfeiffer-George Clooney romantic comedy One Fine Day. Since then, the actress has continued to build both her film and television credits: in 1997, she appeared in the AIDS drama Touch Me, and the following year she had sizable roles in South Boston crime drama Southie with Donnie Wahlberg and Rose McGowan, which one the American Independent award at the Seattle Film Festival in 1998. On television, she could be seen guest starring on a number of shows, including Seinfeld and Ellen Foster. In 1999 she got her own television show, Jack and Jill, on the WB Network. That same year, she could be seen playing Sean Patrick Flanery's fiancée in Simply Irresistible and then acting as his bedmate in Body Shots, another in the long line of explorations into pre-millennial twenty-something dating angst.

After starring in director Neil Turitz's debut Two Ninas, Peet landed a leading role in Peter M. Cohen's independent comedy Whipped. While the film itself performed dismally, Peet met her boyfriend Brian Van Holt on the set. Despite it's independent status, Whipped was given a solid amount of mainstream marketing, and Peet was praised for a game performance in the face of an admittedly weak script.

After a small role in 2000's Isn't She Great with Bette Midler and Nation Lane, Peet was finally recognized by critics and audiences alike in The Whole Nine Yards. Though the film itself did not fare particularly well, Peet was praised for holding her own against Hollywood heavy-hitter Bruce Willis, which certainly didn't hurt her when it came time to audition for Saving Silverman, which placed her opposite Jason Biggs while he was still reeling from the success of American Pie. In 2002, Peet played a considerably less vicious wife in Changing Lanes with Ben Affleck and Samuel L. Jackson, and won no small amount of praise for her performance as the heroin-addled mistress of Kieran Culkin's character's godfather in Igby Goes Down. Peet would go on to star opposite film veterans Diane Keaton and Jack Nicholson in Nancy Meyers' Something's Gotta Give, in which she stars as Nicholson's scandalously young girlfriend, as well as James Mangold's psychological thriller Identity with John Cusack. In 2004, Peet is slated to appear in the sequel to The Whole Nine Yards (aptly titled The Whole Ten Yards, and act alongside Josh Brolin, Chloe Sevigny, and Gene Saks in a yet unnamed Woody Allen feature. The young actress is also scheduled to play the leading role in John McKay's 2005 romantic comedy Picadilly Jim.