According to Stereogum, Brion's work on Mann's first solo albums "lay the groundwork for a sound that became synonymous with a strain of notable alternative acts at the turn of the century".

[1] Brion's film scores include Hard Eight (1996), Magnolia (1999), Punch-Drunk Love (2002), Eternal Sunshine of the Spotless Mind and I Heart Huckabees (both 2004), Synecdoche, New York (2008), ParaNorman (2012), Lady Bird (2017), and Christopher Robin (2018).

He comes from a musical family; his mother, LaRue, was a singer and administrative assistant, and his father, Keith Brion, was a band director at Yale.

From 1980 to 1985 Jon was part of the band The Excerpts, along with Stephen Harris, Dean Falcone, Jim Balga, Bobby Butcher & Spike Priggen.

He contributed guitar work to Jellyfish's 1993 album Spilt Milk, and in 1994, joined Dan McCarroll, Buddy Judge and ex-Jellyfish guitarist Jason Falkner in the short-lived pop band the Grays.

Brion is featured as keyboardist and drummer on Marianne Faithfull's 2003 album, Kissin Time, and co-wrote a song, "City of Quartz", for her next work, 2005's Before the Poison.

He has also produced albums by Fiona Apple, Rufus Wainwright, Eleni Mandell, Rhett Miller, Robyn Hitchcock, Brad Mehldau and Evan Dando, and co-produced Kanye West's Late Registration in 2005.

[8] According to Stereogum, Brion's work on Aimee Mann's first solo albums "lay the groundwork for a sound that became synonymous with a strain of notable alternative acts at the turn of the century".

He has also scored and provided original music for I Heart Huckabees, Punch-Drunk Love, Step Brothers (with Chris Thile), ParaNorman, The Future, Synecdoche, New York, Greta Gerwig's Lady Bird and Disney's Christopher Robin (with Geoff Zanelli).

Brion is renowned for his regular Friday-night gigs at the Los Angeles club Largo, which feature covers and original songs, a variety of instruments and occasional guest musicians and comedians.

He uses a "jigsaw puzzle" approach to performing songs, and uses looping systems to record himself starting often with drums, then adding piano, bass, guitar, and vocals.

Over the years, shows have featured spontaneous appearances with Jackson Browne, Gillian Welch, Fiona Apple, Rickie Lee Jones with upright bassist Stephen Patt (ex-The Chambers Brothers), Aimee Mann, Elliott Smith, Ben Folds, Nels Cline, percussionist Matt Chamberlain, Tori Amos, bassist Sebastian Steinberg (ex-Soul Coughing), and fiddler Sara Watkins (Nickel Creek).