Murdoch taught philosophy at Oxford from 1948-63. In 1956, she married the academic and literary critic John Bayley, later Warton Professor of English at Oxford. In 1954, her first published novel, Under the Net, was acclaimed as a comic masterpiece. Her subsequent works, while lacking the spontaneous humour of Under the Net, revealed qualities which soon established her as one of the most important writers of her time.

In 1958, The Bell was published, considered by many critics to be her finest novel. Set in a quasi-religious community in an ancient country mansion, this embodies many of the characteristic features of her work: intricate melodrama, serious philosophical debate, complicated sexual relationships, a bold use of symbolism, a plot that combines macabre, fantastical and richly comic incidents and a tone that, while not strictly realistic, accurately portrays the social and intellectual life of the mid 20th century.

Murdoch was at her peak in the novels of the 1960s and the 1970s, notably with A Severed Head, The Red and the Green, The Italian Girl, The Nice and the Good, A Fairly Honourable Defeat, The Black Prince and A Word Child. Characters in Iris Murdoch novels are driven by irrational impulses, unconscious fears, social pressures and dark exterior forces, but they continue to believe that they are in control of their lives and behaviour. She was made a Dame of the British Empire in 1987. Murdoch also showed skill as a playwright, working with J B Priestley to dramatise A Severed Head in 1963, and with James Saunders in the dramatisation of The Italian Girl in 1967. Many of her philosophical and political themes were summarised in Metaphysics as a Guide to Morals, published in 1992.