Jon Brion was born on December 11, 1963, in Glen Ridge, New Jersey. He comes from a musical family, with his mother, LaRue, being an administrative assistant and singer, and his father, Keith Brion, being a band director at Yale. His brother and sister became a composer/arranger and a violinist, respectively. Brion grew up in Connecticut, where he dropped out of Hamden High School at the age of 17 to pursue a music career.
Jon Brion was part of several bands before becoming a successful producer and film score composer. He was part of the band The Excerpts from 1980 to 1985, and later formed the band The Bats with Bill Murphy and Don "Riff" Fertman. The Bats released a single and an album, but disbanded due to lack of commercial success.
In the 1980s, Brion also played solo gigs, formed the band World's Fair, and became a member of Aimee Mann's band 'Til Tuesday. He contributed guitar work to Jellyfish's album Spilt Milk and played guitar on the Wallflowers' hit song "One Headlight".
Brion's work as a producer and composer began in the 1990s. He produced music for artists such as Of Montreal, Aimee Mann, Love Jones, Eels, Fiona Apple, Elliott Smith, Robyn Hitchcock, Rhett Miller, The Crystal Method, Kanye West, Sky Ferreira, and Mac Miller. He also composed film scores for movies such as Hard Eight, Magnolia, Punch-Drunk Love, Eternal Sunshine of the Spotless Mind, and Synecdoche, New York.
Brion has released several albums, including his debut solo album Meaningless in 2001. He has also collaborated with other artists, including Marianne Faithfull, Rufus Wainwright, and Brad Mehldau.