John Cairney made his stage debut at the Park Theatre, Glasgow, before enrolling at the Royal Scottish Academy of Music and Drama (RSAMD) in Glasgow. After graduation, he joined the Wilson Barrett Company as Snake in 'The School for Scandal'. A season at the Glasgow Citizens' Theatre followed before going on to the Bristol Old Vic where he appeared in the British premiere of Arthur Miller's 'The Crucible'. He returned to the Citizens from time to time, most notably as Hamlet in 1960. He also appeared in the premiere of John Arden's 'Armstrong's Last Goodnight' in 1964.
Other stage work until 1991 included King Humanitie in 'The Thrie Estaites' for Tyrone Guthrie at the Edinburgh Festival, Archie Rice in 'The Entertainer' at Dundee (1972),as the title character in 'Cyrano de Bergerac' at Newcastle (1974),Becket in 'Murder in the Cathedral' at the Edinburgh Festival of 1986 and 'Macbeth' in the same Festival in 1989.