Oldham began his acting career at age 17, when he portrayed a teen preacher in John Sayles's film about an Appalachian mining community, Matewan (1987). Oldham moved to Hollywood to pursue acting in the late 1980s, and landed roles in a couple of films. However, he quickly became disillusioned with the film industry and quit in 1989. He has since had several minor roles in independent films, such as Julien Donkey-Boy (1999), Junebug (2005), and The Guatemalan Handshake (2006). Oldham took a lead role in Old Joy, which was featured at SXSW XX and opened at New York's Film Forum on September 20, 2006. During this time, he also played the role of a preacher in the "Horse Apples" special of WonderShowzen in series 2 of the show. In 2007, Oldham starred alongside Zach Galifianakis in the alternate music video for Kanye West's Can't Tell Me Nothing. In 2009, he was the narrator of "Madam and Little Boy", a documentary film about atomic weapons directed by Swedish Artist Magnus Bärtås. In 2010, Oldham had a small part in Jackass 3D as a gorilla trainer. He revealed that he had to write a theme song in the style of a Saturday morning cartoon show for filmmaker Lance Bangs' life to get the role.