He has starred as Jimmy James on the NBC sitcom NewsRadio (1995–1999), as Milton Waddams in the film Office Space (1999), and voiced Bill Dauterive and Buck Strickland on the animated series King of the Hill (1997–2010).

Other notable film roles include Dave (1993), Dodgeball (2004), Idiocracy (2006), Cedar Rapids (2011), Selma (2014), Trumbo (2015), Get Out (2017), and On the Basis of Sex (2018).

K'Vada in the Star Trek: The Next Generation two-part episode "Unification" (1991) and Hawthorne Abendsen in seasons 2–4 of the series The Man in the High Castle.

He has supporting roles in a variety of HBO series, including Boardwalk Empire, True Blood, Perry Mason, and Succession.

Root has likened his childhood to that of an Army brat, as his family frequently relocated while his father finished each construction project.

He appeared in many comedy films, particularly as the mumbling, quirky Milton Waddams in Office Space;[6][5] the mild-mannered gym rat Gordon Pibb in Dodgeball: A True Underdog Story; Suds, a drunk sportswriter, in Leatherheads; and the dimwitted principal in the 2008 Judd Apatow-produced comedy Drillbit Taylor.

Root reunited with Mike Judge in Idiocracy and has also portrayed NASA flight director Chris Kraft in the miniseries From the Earth to the Moon.

He also had a regular role on the short-lived CBS series Ladies Man, which starred Sharon Lawrence soon after she left NYPD Blue.

He played Raymond, a hunting store owner involved in illegal gun trading, in the 1993 In the Heat of the Night episode "A Love Lost."

He has also provided vocal talent in animated television series such as Chowder, Batman: The Brave and the Bold, and Teen Titans.

He appeared as Johnny Forreals, inventor of the word "boo-yah," on "Cangamangus", an episode of The Sarah Silverman Program on Comedy Central.