Born Francesco Rosario Capra in Bisacquino, Sicily, Italy, Capra moved with his family to America in 1903, settling in Los Angeles, California, where he graduated from Throop Institute (later renamed the California Institute of Technology) with a B.S. degree in chemical engineering. On October 18, 1918, he joined the United States Army. While at the Presidio, he got Spanish influenza and was discharged on December 13. In 1920, he became a naturalized citizen of the United States.

Like other prominent directors of the thirties and forties, Capra began his career in silent films, notably by directing and writing silent film comedies starring Harry Langdon and the Our Gang kids. In 1930 Capra went to work for Mack Sennett and then moved to Columbia where he formed a close association with screenwriter Robert Riskin (husband of Fay Wray) and cameraman Joseph Walker. However, in 1940 Sidney Buchman replaced Riskin as writer.

After the 1934 Oscar winning romantic comedy It Happened One Night, Capra directed a steady stream of films for Columbia intended to be inspirational and humanitarian. The best known are Mr. Deeds Goes to Town, the original Lost Horizon, and Mr. Smith Goes to Washington. His ten year break from screwball comedy ended with the comedy classic Arsenic and Old Lace.

Between 1942 and 1948, when he produced State of the Union, Capra also directed or co-directed eight war documentaries including Prelude to War (1942), The Nazis Strike (1942), The Battle of Britain (1943), Divide and Conquer (1943), Know Your Enemy Japan (1945), Tunisian Victory (1945) and Two Down and One to Go (1945). His Academy Award-winning documentary series, Why We Fight, is widely considered a masterpiece of propaganda, surpassed only by Leni Riefenstahl's Triumph of the Will; Capra was faced with the task of convincing an isolationist nation to enter the war, desegregate the troops, and ally with the Russians, among other things.

Capra's 1946 It's a Wonderful Life (another inspirational and humanitarian themed film) was the first picture for Jimmy Stewart after his service in World War II. The film was ignored on its initial release, but it became a favorite for television progamming on Christmas Day after its copyright expired.

Capra's final theatrical film was 1961's Pocketful of Miracles, with Glenn Ford and Bette Davis. He had planned to do a science fiction film later in the decade but never even got around to pre-production, but he did end up producing several television specials for the Bell Telephone System dealing with science.

In 1971, Capra published his autobiography, The Name Above the Title. Though unreliable in its details, it offers a compelling self-portrait.

Capra was also the subject of a 1991 biography by Joseph McBride entitled Frank Capra: The Catastrophe of Success. McBride corrects many of the impressions left by Capra's autobiography.

Capra won an Academy Award for Directing in 1934 for It Happened One Night, in 1936 for Mr. Deeds Goes to Town, and in 1938 for You Can't Take It with You. It Happened One Night and You Can't Take It with You also won an Academy Award for Best Picture.

Frank Capra passed away in La Quinta, California of a heart attack in his sleep in 1991 at the age of 94 and was interred in the Coachella Valley Cemetery, Coachella, California.

His producer and son, Frank Capra, Jr., is president of Screen Gems, in Wilmington, North Carolina, one of the three children born to Capra's second wife, Lou Capra. Frank Capra's grandson is Frank Capra III, and his great-grandson Francis Capra plays the role of Eli "Weevil" Navarro on the popular series Veronica Mars.

Quote from Capra: "There are no rules in filmmaking, only sins. And the cardinal sin is dullness."