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Barry Oakley was educated at the Christian Brothers College, St Kilda and the University of Melbourne. In the 1950s and 1960s he worked as a secondary school teacher (1955-1962), lecturer in humanities at the Royal Melbourne Institute of Technology (1963), an advertising copywriter (1964-65) and a copywriter for the federal Department of Trade and Industry (1966-73). During this time a number of his short stories were published in journals such as Southerly, Meanjin and Quadrant (qq.v). In 1967 Oakley published his first novel, A Wild Ass of a Man, and saw his first play performed. In 1970 he was the joint winner of the Captain Cook Bicentenary Literary Award for the novel Let's Hear It for Prendergast, but he is most admired for his dramatic works.
Oakley's earliest plays were performed at Melbourne's La Mama Theatre and he associated with several members of the Australian Performing Group, including John Romeril, Jack Hibberd and David Williamson . Oakley's Melbourne settings and characters, and the comic and satiric presentation of experiences familiar to Melbourne audiences made his plays popular and regularly performed during the 1970s. This established his reputation as a significant commentator on the effects of power and submission in a variety of social situations.
In 1988 Oakley began his nine-year term as literary editor of The Australian, a period where he held considerable influence in the development of Australian writing. Oakley has received grants from the Australia Council and has been writer-in-residence at several universities. He has lived with his wife in the Blue Mountains, New South Wales.