His 200-plus acting credits include feature films such as The Waterboy and Apollo 13, as well as television series, such as Gentle Ben, The Baileys of Balboa, The Cowboys, My Name Is Earl, and several entries in the Star Trek franchise.

Howard began his career when he was two, appearing in five episodes of The Andy Griffith Show, then starring his older brother Ron.

In 1963, Howard appeared in the ABC medical drama Breaking Point in the role of four-year-old Mikey in the episode "The Gnu, Now Almost Extinct".

[3][4] In 2024, Howard appeared on the CBS soap The Bold and the Beautiful as Tom Starr, a homeless man who turned his life around, only to be murdered.

Other roles in the elder Howard's films include: John Dexter in Cocoon (1985), Paul in Gung Ho (both film and TV series), pathologist Ricco in Backdraft (1991), Lou in Parenthood, Flynn in Far and Away (1992), flight controller Seymour Liebergot in Apollo 13 (1995), Ken in EDtv (1999), Whobris in How the Grinch Stole Christmas (2000), and Harry the referee in Cinderella Man (2005).

Howard also played Sheriff Purdy in The Missing (2003), Lloyd Davis in Frost/Nixon (2008), Herbert Trimpy in The Dilemma, and Paul Lucas in the episodes "Spider" and "We Interrupt This Program" of the HBO miniseries From the Earth to the Moon, which was produced by Ron.

Howard played Eaglebauer in Rock 'n' Roll High School, Usher in Get Crazy, Paco in The Waterboy, Arthur Lynne in Uwe Boll's Heart of America, cellmate Slinky in Tango & Cash, KJZZ disk jockey in That Thing You Do!, Johnson Ritter in the Austin Powers series, another flight controller in Night at the Museum: Battle of the Smithsonian, Nipples in Little Nicky (2000), Gregory Tudor in the low budget film Ice Cream Man (1995), Rughead in The Wraith (1986), Stanley Coopersmith in Evilspeak (1981), Kate the Caterer in The Cat in the Hat (2003), Doctor Koplenson in Halloween (2007), and appeared in the romantic comedies, Play the Game and Speed-Dating.

[11] On January 29, 2016, three days before the Iowa Caucuses, he endorsed United States Senator Ted Cruz of Texas for the Republican presidential nomination.