Hackett's earliest musical influences came from Johann Sebastian Bach and opera singer Mario Lanza. He has said that his compositions are still influenced by them.
Later, numerous British blues artists were examples for him, such as Danny Kirwan, Peter Green and several guitarists from John Mayall & the Bluesbreakers, he was also influenced by Jimi Hendrix, The Beatles and King Crimson.
Before joining Genesis in 1970, where he replaced guitarist Anthony Phillips, he played in several rock bands.
Hackett's first recording with Genesis was Nursery Cryme (1971). He helped shape the group's sound by strongly encouraging them to incorporate a Mellotron into the songs, and his guitar work is prominently featured through solos on "The Musical Box", "The Return of the Giant Hogweed", and "The Fountain of Salmacis".
He became an early proponent of the guitar tapping technique.
After recording his debut album Voyage of the Acolyte , Hackett resumed working in Genesis and recorded several more albums with them.
After the Wind & Wuthering tour, Hackett left the band during the mixing stage of the Genesis live album, Seconds Out. His departure was announced in the press during the promotion of the album on 8 October 1977.
Hackett's first post-Genesis album was Please Don't Touch!, released in 1978. As with Voyage of the Acolyte (1975), much of the material on the album was in the style of progressive rock. It did contain, however, much more vocal work. Hackett, who had never sung lead or backing vocals on a Genesis song, turned over most of the vocals to a number of singers, including folk singer Richie Havens, R&B singer Randy Crawford, and Steve Walsh of American progressive rock group Kansas.
Hackett releases another 20 albums and still performs mainly with Genesis compositions.