Wilson's film acting career began with the lead role in the film Bottle Rocket in 1994, which was co-written by Wilson's older brother Owen and director Wes Anderson. Bottle Rocket was later made into a feature-length film in 1996.

After moving to Hollywood with his two brothers, he was cast opposite Calista Flockhart with romantic designs in Telling Lies in America and made a cameo appearance in the film-within-the-film of Scream 2 (both 1997). Wilson filmed back-to-back romantic films opposite Drew Barrymore, Best Men, about a group of friends who pull off a heist on their way to a wedding, and Home Fries (both 1998), about two brothers interested in the same woman for very different reasons. (Off-screen, the actor won the girl; he and Barrymore became a couple, but parted ways in 1998.) Wilson remained in demand, playing the doctor beau of a schoolteacher in Rushmore (also 1998), directed by Anderson and co-written by brother Owen.

A starring role opposite Reese Withe