Although he had made two German films in New York, Root began to win parts in and film projects after "All My Sons". His first American feature was George Romero's "Monkey Shines: An Experiment in Fear" (1988), in which he was a cold-blooded scientist trying to steal a serum. He followed by playing a police sergeant none too sympathetic to Demi Moore in "Ghost" (1991) and Gary Murray in the send-up "Buffy the Vampire Slayer" (1992).
On TV, Root did small roles in such longform fare as "Cross of Fire" (NBC, 1989) and numerous episodic roles. Perhaps his best-known role was as Kevin McDonald, who, with his wife, provides stability for the children whose mother has murdered their father in "A Woman Scorned: The Betty Broderick Story" (CBS, 1992) and its same-year sequel, "Her Final Fury: Betty Broderick The Last Chapter". In 1993, he won the role of ranch hand R.O. Moon on the series "Harts of the West" (CBS). After its demise Root was cast in his most beloved role, as the unflappable station owner Jimmy James on the sitcom "NewsRadio" (NBC, 1995-1999) where his comedic abilities were allowed to flourish unchecked. As a voice actor, Root was also a cast on another influentail and longer-running TV comedy, providing the voices of Hank Hill's patheticly loveable neighbor Bill Dauterive on creator Mike Judge's animated series "King of the Hill" (Fox, 1997 - )--Root also voiced Hank's boss Buck Strickland and dozens of other characters over the course of the series' run.
Judge also tapped Root to co-star in his first live-action effort as writer-director "Office Space" (1999), which failed to ignite big box office but later soared to new heights as a beloved cult classic comedy, due in no small part to Root's performance as about-to-snap office drone Milton Waddams. Back on the small screen, Root had a memorable dramatic turn as NASA flight director Chris Kraft in the Tom Hanks-produced HBO miniseries "From the Earth to the Moon" (1998) and joined the cast of the short-lived Alfred Molina sitcom "Ladies Man" (CBS, 1999-2000).
Root soon became a favored supporting player on the big screen as well, appearing in such films as "Bicentennial Man" (1999), "White Oldeander" (2002) and "Jersey Girl" (2004). After appearing in a highly amusing role as a blind Southern disc jockey in "O Brother, Where Art Thou?" (2000), Root also found himself added to the Coen Brothers' recurring cast of eccentrics, joining them again for "The Ladykillers" (2004) as Marlon Wayans' easily flattered supervisor. Root added another memorably awkward and nerdy misfit to his resume with his role as Gordon in the comedy "Dodgeball" (2004).
Along with "King of the Hill," Root can be heard as a voice actor in such projects as "The Big Guy and Rusty the Boy Robot," "Ice Age" (as the Rhino), Disney's "The Country Bears" (as Zeb) and Disney/Pixar smash hit "Finding Nemo" (as Bubbles).