John Riddoch Poynter graduated from the History Department at the University of Melbourne and pursued further studies at Oxford as a Rhodes Scholar from 1951 to 1953. After returning to the Universtiy of Melbourne Poynter taught at Trinity College and in the Social Studies Department, rejoining the History Department in 1963. He was Ernest Scott Professor of History from 1966 to 1975 and Deputy Vice-Chancellor from 1975 to 1990.
Poynter also wrote The Enterprises of F. S. Grimwade and His Sons (1966), for the Business Archives Council of Australia, Society and Pauperism : English Ideas on Poor Relief, 1795-1834 (1969) and A Place Apart : The University of Melbourne : Decades of Challenge (1996).
