In 1975, when lead singer Peter Gabriel left Genesis, Collins took over as vocalist. The band enjoyed its most commercially successful period with Collins as vocalist, and in 1986 Invisible Touch topped the album charts. By this time they had several hit singles under their belt to go with the string of successful albums. Collins finally left Genesis in 1996.
During the 1970s Collins also played drums for the jazz fusion band Brand X. In the 1980's he did session drumming for such high-profile acts as Robert Plant and Tears for Fears. He also has collaborated with well known musicians, such as George Harrison, Paul McCartney, Robert Plant, Eric Clapton, Mike Oldfield, and several others.
In 1981, Collins had embarked on a simultaneous solo career with the album Face Value. In 1985 he was one of the stars of the Live Aid concert during which he was jetted from Britain to the USA on the Concorde to take part in both parts of the programme. He also took up acting again, taking the lead in the 1988 flop Buster, in which he played train robber Buster Edwards.
Collins is a successful songwriter, and was asked by The Walt Disney Company to produce the score for the animated film Tarzan in 1999. His song "You'll Be in My Heart" won an Academy Award.
Collins does not read and write conventional musical notation but uses a system of his own devising. In recent years he has reportedly been losing his hearing in one ear, and in 2003 announced a farewell tour.