He was born in New Jersey. Before forming A Perfect Circle, Howerdel worked as a guitar tech for Faith No More, Fishbone, David Bowie, The Smashing Pumpkins, Nine Inch Nails, Guns N' Roses, and numerous other bands.
Howerdel functioned as a roadie and Pro Tools technician for Tool during the tour and recording of Ænima, working with Maynard James Keenan, whom he met in 1992. During this time, Howerdel played Keenan some of his songs, and Keenan offered his vocals if Howerdel ever decided to form a band. Despite originally considering a female singer, Howerdel would eventually accept Keenan's offer. In 1999, Howerdel founded A Perfect Circle, and invited Keenan to join in as the singer. In 2006, Keenan explained in an interview conducted by French magazine "Rock Hard", that A Perfect Circle is not only on hiatus, but finished.
Howerdel has occasionally played live with the band Abandoned Pools. In 2005, he wrote and recorded music for the video game Jak X: Combat Racing, which also features remixes of Billy's songs by Danny Lohner, and musicians Josh Freese and Troy Van Leeuwen of Queens of the Stone Age, Atom Willard of The Offspring, Joey Castillo of Queens of the Stone Age, ex-A Perfect Circle bassist Paz Lenchantin, and Wes Borland of Black Light Burns. Howerdel is currently working on a new album- "I don't know if you'd call it a solo album or a new band." (Oct. 6, 2005 GameSpy interview)
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