Cowsill has played keyboards for the Beach Boys touring band performing Al Jardine's and the late Carl Wilson's vocal parts.

In the wake of Beatlemania, John and three of his brothers, Bill, Bob, and Barry, formed their own group solely based around the Liverpool band.

John performed mainly backing vocals, although he sang lead on "Silver Threads and Golden Needles".

[3] His solos for the concerts include "Wild Honey", "Sail On, Sailor", "Darlin'" and "California Dreamin'" on the 2022 tour.

[4] Cowsill appears on the band's subsequent studio album, That's Why God Made the Radio (2012).

In a podcast recorded April 26, 2023, John said: "A guy, Scott Totten - who is the musical director of the Beach Boys, and I got let go four days ago.

So, I play really well.”[5] In 2017, Cowsill joined with Vicki Peterson and Bill Mumy as the band Action Skulls to release an album (also including posthumous contributions from the bassist Rick Rosas) entitled Angels Hear.