In 2003, he was awarded the National Medal of Arts.

Howard was born in Duncan, Oklahoma, the son of Jean Speegle Howard, an actress, and Rance Howard, a director, writer, and actor. His family moved to Burbank, California in 1958, the year before the birth of his younger brother, Clint Howard. Howard graduated from John Burroughs High School, and later attended the University of Southern California's School of Cinematic Arts but did not graduate.

In 1959, he had his first credited film role, in The Journey, and appeared in June Allyson's CBS anthology series The DuPont Show with June Allyson in the episode "Child Lost," as well as The Twilight Zone episode "Walking Distance", about a man (Gig Young) who learns that he cannot go home again.

In 1960, he was cast in the role of Opie Taylor in the hit CBS television series The Andy Griffith Show, a spin-off of The Danny Thomas Show. Credited as "Ronny Howard," he portrayed the son of the local sheriff, played by Andy Griffith, in the fictional town of Mayberry, North Carolina for the entire eight seasons of the show. He also spent a lot of time with Griffith off-screen.

Howard played Winthrop Paroo, the child with the lisp in the 1962 film version of The Music Man with Robert Preston and Shirley Jones. He also starred in the 1963 film The Courtship of Eddie's Father with Glenn Ford and (billed as "Ronny Howard") in Little Boy Lost, a 1963 episode of the NBC medical drama The Eleventh Hour as the character Barry Stewart in the episode entitled "Is Mr. Martian Coming Back?", and a 1966 episode of the NBC adventure series I Spy with Robert Culp and Bill Cosby. Howard made a guest-star appearance on the television series M*A*S*H during that show's first season as an underage American serving in the Marines during the Korean War. In the 1970s, Ron Howard appeared in at least one episode of The Bold Ones as a teenage tennis player with an illness.

In 1976, Howard was offered the role of Gillom Rogers in the movie The Shootist, starring opposite Hollywood legend John Wayne. At the time, Howard had no idea that this would be the last pairing of the two, as Wayne would die three years later of cancer; in fact, Howard is often quoted as saying, "About a couple of months after filming wrapped on The Shootist, Duke called me up and said, 'I found a good script, kid . . . it's you and me, or it's nobody." As a token of respect, during the beginning of The Shootist, Howard lent his voice to the beginning montage, which shows Wayne in various clips from his career.

Howard played Steve Bollander in George Lucas' teen movie American Graffiti in 1973. The role led to him being cast as Richie Cunningham in the TV series Happy Days on which, beginning in 1974, he played the likeable "buttoned-down" boy, in contrast to Henry Winkler's "greaser" Arthur "Fonzie" Fonzarelli. In 1977, while still starring on Happy Days, he directed his first film, a low-budget comedy/action film called Grand Theft Auto.

His last significant on-screen role was when he reprised his famous role as Opie Taylor in the 1986 TV reunion movie Return to Mayberry reuniting him with Andy Griffith, Don Knotts, and most of the old cast.

When asked in 2000 if he would ever like to return to acting, he replied "Only if I can act with Cindy Williams again," referring to the actress who played opposite him in American Graffiti. He also starred in a made for TV film called "Like Normal People." which depicted a retarded couple.

Before leaving Happy Days in 1980, Howard made his directing debut with the 1977 project Grand Theft Auto (after cutting a deal with Roger Corman to star in Eat My Dust with Christopher Norris). Howard went on to direct several TV movies. His big theatrical break came in 1982 with Night Shift featuring soon-to-be stars, such as Michael Keaton and Shelley Long, as well as reuniting Howard with Happy Days co-star Henry Winkler.