Born in Los Angeles, John Densmore attended Santa Monica City College and California State University, Northridge.

He joined The Doors in 1965 and remained a member until the band's dissolution in 1973.

Densmore met keyboardist Ray Manzarek and guitarist Robby Krieger at a Transcendental Meditation lecture.

After the Doors' last performance with Morrison in New Orleans in 1970, the band agreed to discontinue performing live.

Densmore allowed "Riders on the Storm" to be used to sell Pirelli Tires, in England only. Densmore later stated that he "heard Jim's voice" in his ears and ended up donating the money earned to charity.

In 2002, Densmore vetoed an offer by Cadillac for $15 million for "Break on Through (To the Other Side)" because of his strong views to conserve the environment.

John Densmore formed a band with fellow ex-Doors Robby Krieger in 1973 called The Butts Band but disbanded after two albums in 1975.

John Densmore left rock and roll in the 1980s, moving to the world of dance as he performed with Bess Snyder and Co., touring the United States for two years. In 1984, at La Mama Theatre in New York, he made his stage acting debut in Skins, a one-act play he had written. In 1985, he won the LA Weekly Theater Award for music with Methusalem, directed by Tim Robbins.

In 1988, he played a feature role in Band Dreams and Bebop at the Gene Dynarski Theatre. He developed and performed a one-man piece from the short story, The King of Jazz, at the Wallenboyd Theatre in 1989. With Adam Ant, he co-produced Be Bop A Lula at Theatre Theatre in 1992. He has acted in numerous TV shows, most memorably as himself in the show Square Pegs, working as a drummer for Johnny Slash's band Open 24 Hours.

His film credits include: Get Crazy with Malcolm McDowell, Dudes directed by Penelope Spheeris, and The Doors directed by Oliver Stone.

As the drummer and an influential member of The Doors, he was inducted into the Rock and Roll Hall of Fame. He worked as a technical adviser on the 1991 film The Doors, and was very impressed with Val Kilmer's performance as Morrison and overall was quite happy with the film.

In 2006, his band, Tribaljazz, released their first album of original work.

Densmore appears alongside Krieger and Manzarek in 2012's RE:GENERATION, a documentary directed by Amir Bar-Lev. It features Densmore collaborating on a new song with Skrillex.

In 2013 Densmore released "The Doors Unhinged", a book covering his legal battle with Krieger and Manzarek over the use of the name The Doors for a tour they were doing, and Densmore's veto over a 2003 offer by Cadillac to buy the rights to The Doors music.