Hunnicutt gained early acting experience in stock theater and entertained in traveling shows. An article in the September 22, 1940, issue of the Brooklyn Daily Eagle reported, "There isn't a decent sized Medicine show traveling through Kentucky, Illinois, Georgia, Indiana or Mississippi, nor a stock company touring those states, which hasn't had the name of Arthur Hunnicutt on its programs." After eight years of such activity, in 1936 he enrolled in a drama school in Cleveland to study theatrical techniques for a year.
Hunnicutt's first film was Wildcat (1942). He appeared in a number of films in the early 1940s before returning to the stage. In 1949 he moved back to Hollywood and resumed his film career. He played a long string of supporting role characters—sympathetic, wise rural types, as in The Red Badge of Courage (1951), The Lusty Men (1952),The Kettles in the Ozarks (1955), The Last Command (1955, as Davy Crockett), The Tall T (1957), Cat Ballou (1965, as Butch Cassidy), El Dorado (1966) and The Adventures of Bullwhip Griffin.
In 1952, he was nominated for an Academy Award for Best Supporting Actor in the Howard Hawks Western, The Big Sky.
Throughout the '50s, '60s and '70s, Hunnicutt made nearly 40 guest appearances on American television programs. He made two memorable appearances on Perry Mason in 1963: he played orange grower Amos Kennesaw Mountain Keller in "The Case of the Golden Oranges," and prospector Sandy Bowen in "The Case of the Drowsy Mosquito." He also made guest appearances on Bonanza, Cheyenne, Gunsmoke, The Outer Limits, The Rifleman, Wanted: Dead or Alive, The Andy Griffith Show, The Wild Wild West, Adam-12, and The Twilight Zone. In one of his last movies, Moonrunners (1975)—the precursor to The Dukes of Hazzard—he played the original Uncle Jesse.
On September 27, 1979, Hunnicutt died of cancer at the Motion Picture & Television Country House and Hospital at age 69. He was buried in the Coop Prairie Cemetery in Mansfield, Arkansas. He was survived by his wife.
