Payne has worked and recorded with J. J. Cale, Jimmy Buffett, Doobie Brothers, Emmylou Harris, Bryan Adams, Pink Floyd, Bob Seger, Toto, Linda Ronstadt, Jackson Browne, Carly Simon, James Taylor, Bonnie Raitt, Helen Watson, Stevie Nicks, Robert Palmer, Richard Torrance, Stephen Bruton, and Shocking Edison. He was a guest performer on Bonnie Raitt's album Sweet Forgiveness in 1977, and wrote its track, "Takin' My Time."
Paul Barrere and Bill Payne played several live concerts with Phil Lesh and Friends, from October 1999 through July 2000. Payne was a member of Boulder band Leftover Salmon from 2014 until December 2015.
In August 2015, Payne was selected to play keyboards for The Doobie Brothers after their keyboardist Guy Allison was called to work on an album project in Japan. However, in December 2015 Payne rejoined the Doobies as a touring member, officially taking the position previously held by Allison. In the few weeks of touring with the Doobies, he was featured with the band and Michael McDonald on The Tonight Show Starring Jimmy Fallon. Payne's temporary term ended in early September after the Doobies' concert at the BB&T Pavilion in Camden, New Jersey.

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