Francis Barrett Faulkner was born on July 12, 1881 in Keene, New Hampshire. He attended Phillips Exeter Academy and went on to study at Harvard College. Around this same time, Faulkner began an apprenticeship with his cousin and painter Abbott Handerson Thayer and painter George de Forest Brush. He also met sculptors James Earle Fraser and Augustus Saint-Gaudens, both of whom became Faulkner's lifelong friends.
In 1901, Faulkner traveled to Italy for the first time with Thayer and his family. He returned to New York in 1902 and studied at the Art Students League and Chase School. He also completed illustration work for Century magazine.
In 1907, Faulkner won the Rome Prize Fellowship from the American Academy in Rome. shortly thereafter, he left to study in Italy for three years, studying with George de Forest Brush and befriending sculptor Paul Manship. Upon his return in 1910, he started working on his first mural, commissioned by the wife of railroad executive E.H. Harriman. Having found his niche, Faulkner continued taking mural commissions until his career was interrupted by World War I and his service in the camouflage section of the army. Shortly after the war, he completed a mural for the marine headquarters in Quantico, Virginia.
Between 1923-1924, Faulkner worked in collaboration with Eric Gugler and Paul Manship to create the American Academy in Rome war memorial. Also following the war, Faulkner completed murals for the Eastman School of Music in 1922, the Rockefeller Center in 1932, and the National Archives in 1936. That same year, Faulkner bought and refurbished a house named "The Bounty" in Keene, New Hampshire, and built a studio nearby. In 1930, he was elected as a trustee of the American Academy in Rome.
During the 1940s, Faulkner created murals for numerous public buildings and sites around New Hampshire including the Senate Chambers in Concord, the Elliot Community Hospital, Keene National Bank, and the Cheshire County Savings Bank in Keene. During his final decades, Faulkner wrote an unpublished manuscript on the history of art in the Connecticut River Valley entitled A Neighborhood of Artists, and his posthumously published memoirs, Sketches of an Artist's Life. Faulkner died in 1966, in Keene, New Hampshire.