Running from 1989 to 1994, the show earned a devoted following and several Emmy nominations. A contributing writer to the ... show, Foley also appeared in the cast. Some of his best characters include Manservant Hecubus, Bruno Puntz Jones, and the insane Jerry Sizzler. After the show's cancellation, the group stayed in contact for the 1996 feature Kids in the Hall: Brain Candy and the 2001 live tour Kids in the Hall: Same Guys New Dresses.

Relocating to Los Angeles, Foley appeared in the unfortunate movie It's Pat and went to work on a new television show, starring as station manager Dave Nelson in the aptly named sitcom NewsRadio from 1995 to 1999. During this time, he also wrote, produced, and starred in the comedy The Wrong Guy, which won Best Screenplay at the U.S. Comedy Arts Festival.

Working in Hollywood, he had supporting parts in the comedies Hacks, Blast From the Past, and Dick. Meanwhile, he provided the voice of Flik the Ant in A Bug's Life, Toy Story 2, and It's Tough to Be a Bug, as well as various voices in the South Park movie, the IMAX movie CyberWorld, and the miniseries From the Earth to the Moon. Mixing animation with his sketch comedy background, he then starred in Monkeybone, based in part on the graphic novel Dark Town. On-stage, he appeared in the musical comedy White Trash Wins Lotto, which ran at The Roxy in Hollywood.

He also had supporting parts in the comedy features On the Line, Run Ronnie Run!, and Stark Raving Mad. In 2003, Foley returned to his native Canada to appear in the comedy Whitecoats, directed by Dave Thomas.