Peter Bowles started his career with the Old Vic Company in 1956 playing small parts in Macbeth, Romeo and Juliet, Troilus and Cressida and Richard II. After a season this company toured North America, concluding with a sell-out season at the Winter Garden Theatre on Broadway. He played in many performances at the Bristol Old Vic.
Bowles was warned by casting directors on leaving RADA that because of his swarthy looks he would never play an Englishman. Indeed, his early career in television consisted mostly of playing foreign villains in such shows as The Avengers (Bowles featured in four series), Danger Man, The Saint, The Persuaders! and The Prisoner (in which he played 'A').
Bowles' final villainous role, on television at least, was playing Balor ('the most evil man in the universe') in an episode of Space: 1999. He also appeared as Caractacus in the TV adaptation of I, Claudius (1976). His first major English role was Guthrie Featherstone QC MP, whom he played in many series of Rumpole of the Bailey (1970–1980).
After playing his first comedy role on TV (Hilary) in an episode of Rising Damp, Bowles was often seen as a comedy actor and parts in comedy series such as Only When I Laugh, The Bounder, Executive Stress and To the Manor Born followed; however, he turned down The Good Life.
The outstanding popularity of To the Manor Born, which had audiences of over 20 million for all twenty-one episodes, changed Bowles' life. After being told by the BBC his success in comedy meant he would never work in drama again, Bowles devised a drama series called Lytton's Diary, which he sold to ITV. It was while starring in this that he was offered the title role of Major Yeates in the hugely successful TV series The Irish R.M. for Channel 4. A headline in the Evening Standard after that series' success read ‘Bowles Saves Channel 4'.
Much of Bowles' work was now being shown on American television, including PBS's Masterpiece Theatre, and he was very flattered to discover that admirers in America of his work included Stephen Sondheim, Quentin Tarantino and Marlon Brando. Following The Irish R.M., Bowles co-devised the comedy/drama series Perfect Scoundrels, which ran for three series on ITV.