Funk joined the Decemberists after meeting Colin Meloy at a solo show Meloy was performing. He has been a member of the band since its formation, appearing on every Decemberists record since. Funk most commonly contributes guitar, pedal steel, and mandolin tracks to the band's songs, though he has laid down tracks with several other instruments as well. After an incident in which the band's equipment trailer was stolen in 2005, Funk wrote "This Machine Kills Thieves" on his banjo, in reference to Pete Seeger and Woody Guthrie.
He is a member of Knock-knock with DJ Rev. Shines (from the hip-hop group Lifesavas on Quannum Projects). He is also a member of the string band Black Prairie who released their first album, Feast of the Hunter's Moon, in 2010. He plays in the country rock group Blue Giant. He has produced records for Stephen Malkmus & the Jicks, Kyle Craft, The Builders and The Butchers, Langhorne Slim, and Red Fang.
On December 20, 2006, Funk appeared on Comedy Central's The Colbert Report to end a longstanding mock feud with the show's host, Stephen Colbert. A contest ensued in which Funk and Colbert would each play a guitar solo while a panel of judges decided the winner. After Funk's solo, Colbert (who cannot play the guitar) feigned an injured hand, having Peter Frampton fill in for him instead. The contest ended with Colbert/Frampton being decided the winners by show guests Eliot Spitzer and Henry Kissinger, and Colbert was awarded The Crane Wife by The Decemberists as the grand prize. Funk then performed an "all-guitar jam" alongside Frampton, Robert Schneider (of The Apples in Stereo), and Rick Nielsen.