He attended Brown University sporadically while pursuing a career as an actor, and living between Brooklyn, Los Angeles, and Bloomington, Indiana.

[7] He began making music during this time, initially as a project for his professor Jeff Todd Titon, an ethnomusicologist at Brown University.

He has been called an "Appalachian post-punk solipsist",[9] with a voice that has been described as "a fragile sort-of warble frittering around haunted melodies in the American folk or country tradition.

Beginning in 1998, Oldham has primarily used the moniker Bonnie 'Prince' Billy, which draws inspiration from several sources: [T]he name has so many different references that it could almost have a life of its own.

[18] The project was never picked up by a television network, but the short with Oldham finally saw official release in the 2015 retrospective box set Digging My Own Grave: The Films of Caveh Zahedi.

As part of an agreement to play that role, he wrote a theme song, in the style of a Saturday-morning cartoon show, for filmmaker Lance Bangs.

[23] In 2011, Oldham played a father telling a bedtime story to his son in David Lowery's short film Pioneer.

In 2009, Oldham narrated Madam and Little Boy, a documentary film about atomic weapons, directed by Swedish artist Magnus Bärtås.

In 2010, Oldham narrated Music Makes a City, a documentary about the formation of the Louisville Orchestra, directed by Owsley Brown III and Jerome Hiler.

[25] Oldham provided voice work and inspiration for the character "Will" in the video game Kentucky Route Zero, released in 2013.