After touring through the spring of 1996, the band Foo Fighters entered a Seattle studio with producer Gil Norton to record its second album. Conflict erupted between Dave Grohl and then drummer, William Goldsmith, eventually causing Goldsmith to leave the band. They regrouped in Los Angeles and almost completely re-recorded the album with Grohl on drums. The album, The Colour and the Shape, was released on May 20, 1997. Hawkins called up Grohl, as he was aware Foo Fighters was in need of a new drummer. Hawkins then auditioned for the band and became a member. He made his Foo debut in time for the album's release.

In addition to his drumming duties with the Foo Fighters, Hawkins is also an accomplished rock singer, guitarist and pianist and took over lead vocals for Foo Fighters on "Cold Day in the Sun," a song on the acoustic half of the double album In Your Honor which was later released as a single, and "I Feel Free," which appeared as the B-side of "DOA" and on the EP Five Songs and a Cover. Live, he occasionally provides backing vocals and, at times, lead vocals while Dave Grohl plays drums.

Hawkins has said that his drumming has been influenced by Roger Taylor of Queen and Stewart Copeland of The Police. He was voted "Best Rock Drummer" in 2005 by UK drumming magazine, Rhythm.

Hawkins also recorded the drum tracks for the Coheed and Cambria album "Good Apollo, I'm Burning Star IV, Volume Two: No World for Tomorrow", as Coheed and Cambria's drummer Chris Pennie was not able to record due to contractual reasons.

Hawkins latest stint behind the drums can be heard on Eric Avery's first solo effort "Help Wanted" released on Danger Bird Records. Most recently, Hawkins was commissioned to complete an unfinished recording of a song by the late Beach Boys' drummer Dennis Wilson entitled "Holy Man" by writing and singing new lyrics. The recording was released in June 2008 as part of a deluxe edition of Wilson's lone 1977 solo album, Pacific Ocean Blue.

He can also be heard drumming on Foo Fighters band-mate Chris Shiflett's other project, Jackson United's latest album 'Harmony & Dissidence' along with Dave Grohl.