Hawkey was the third member to join Deadsy after frontman Elijah Blue Allman sent him a Juno-106 synth and a demo tape made by Allman and Drummer Alec Puro. Each member of the band represented a color and "entity", with Hawkey's being yellow and science and Medicine, respectively. The members also had their own unique appearance; Hawkey would dress in medical scrubs. On August 1, 1996, Deadsy released their self-titled debut album on the music label Sire Records. In 1999, Deadsy received attention from labels and notable Musicians, with their first gig at The Viper Room attracting members of Limp Bizkit, Orgy, Sugar Ray, and Thirty Seconds to Mars.

The band's second studio album, Commencement, was released on May 14, 2002, and was their debut record released on a major music label after signing to Jonathan Davis' Elementree Records, a division of DreamWorks Records. In addition to playing the synthesizer on Commencement, Hawkey also programmed and played guitar on a number of the tracks. The band subsequently released their first music video, for the song "The Key to Gramercy Park", with Davis providing guest vocals on the track and Fred Durst directing. That same year, Deadsy was invited by Korn to join the Family Values Tour, along with Puddle of Mudd, Stone Temple Pilots, and Linkin Park.

Prior to being a film Producer, Hawkey had a cameo role as a musician in the musical comedy film The Singing Detective (2003). As a film Producer, Hawkey has worked on the drama film Higher Ground (2011), directed by his wife Vera Farmiga, in which he was also an uncredited and unnamed extra. In 2015, he appeared in the first, seventh, and eighth episodes of the Carlton Cuse-produced A&E supernatural drama series The Returned in the supporting role of Paul Koretsky, a father grieving the death of his son in a fatal bus crash. He served as an executive Producer on the documentary film Unspoken (2017).

In 2002, Hawkey also worked with Thirty Seconds to Mars on their self-titled debut album, playing the synthesizer on the song "Capricorn (A Brand New Name)". Deadsy left DreamWorks in 2004, citing its sale to Interscope Records as one of the reasons. In 2006, Deadsy was asked to again join Korn and co-headliners Deftones on the Family Values Tour 2006. The band released their third studio album, Phantasmagore, on August 22, 2006, through Immortal Records. This album would ultimately mark Hawkey's final appearance as part of Deadsy. The band went on hiatus in April 2007, after which Hawkey began a career in carpentry. In 2011, Hawkey served as the music Director to his wife's directorial debut Higher Ground.

In 2004, Hawkey began dating Actress Vera Farmiga after being introduced by mutual friend Allen Hughes on the set of Touching Evil. The couple married in a private ceremony on September 13, 2008, when Farmiga was five months pregnant with their first child. Their son, Fynn McDonnell Hawkey, was born on January 13, 2009 in Rhinebeck, New York. It was announced in April 2010 that Hawkey and Farmiga were expecting their second child. Farmiga gave birth to a daughter, Gytta Lubov Hawkey, on November 4, 2010. The family splits their time between homes in New York City and Vancouver. Through his marriage to Farmiga, Hawkey's sister-in-law is Actress Taissa Farmiga.

In 2011, Hawkey served as musical Director and Producer on his wife Vera Farmiga's directorial debut film Higher Ground, and in 2017, he executive produced the documentary film Unspoken. In 2015, he had a recurring role as Paul Koretsky in the A&E series The Returned.