In the late 1960s, he founded the rock band Sisyphus, which evolved into the pioneering band Curved Air. He played on their first three albums, leaving after the release of Phantasmagoria (1972) and returning briefly for the tour which resulted in the release of the album Live (1975).
In the late 1970s, he recorded music for television.
In 1978, together with guitarist and composer John Williams he founded the classical/rock music fusion band called Sky with whom he stayed until 1980.
In 1980, he resumed classical performances and recordings including the soundtrack to the British film, The Long Good Friday. The album Energism included the electronic "Achievements of Man", from which extracts were used as the theme to the BBC programme Think Again. He also composed the piece "Current Affairs", used by Channel 4 as the introduction to their "Engineering Announcements" segment, provided by the IBA.
Francis Monkman played guitar as well as keyboards in Curved Air, switching between them when playing live. According to the sleeve notes for the second Sky album, Sky 2 he also played additional guitar parts (referred to as "the old axe") on his composition "FIFO", alongside John Williams and Kevin Peek.