Churchill began his career playing piano in cinemas at the age of 15. After dropping out of medical studies at UCLA to pursue a career in music, he became accompanist at the Los Angeles radio station KNX (AM) in 1924.
In 1937, he was chosen to score Disney's first full-length animated feature, Snow White and the Seven Dwarfs. His catchy, artfully written songs played a large part in the film's initial success and continuing popularity.
He became supervisor of music at Disney. In 1942, Churchill and fellow composer Oliver Wallace won an Oscar in the category "Scoring of a Musical Picture" for cowriting the score for Dumbo. He also shared an Oscar nomination with Ned Washington for the song "Baby Mine" from Dumbo for Best Song. A year later, Churchill received two posthumous Oscar nominations; the first for cowriting the score to Bambi with Edward Plumb, and the second for cowriting the song "Love is a Song" from Bambi with lyricist Larry Morey (1905–1971).
Frank Churchill committed suicide on May 14, 1942 at his ranch north of Los Angeles in Castaic. He is purported to have died "at the piano" of a self inflicted gunshot wound. Although there is some speculation that his suicide was a result of negative discourse with Walt Disney regarding his latest scores for Bambi, it was more likely due to his deep depression and bout with heavy drinking after the deaths of two of his closest friends and fellow Disney orchestra members who had died earlier that year within a month of each other. He was buried in Glendale's Forest Lawn Memorial Park Cemetery.