In 1937 he became a member of the Commonwealth Public Service from where he was granted a Commonwealth scholarship to pursue a doctorate at the London School of Economics. He joined the Department of External Affairs in 1941 and served as private secretary to Herbert Vere Evatt. In 1947 he became Secretary of the Department of External Affairs and held that position until mid-1950. At the beginning of 1951 he took up the position of Australian High Commissioner for Ceylon, but resigned to return home and contest the Federal election of that year in the electorate of Lowe. As ALP candidate he was beaten by William McMahon, a future Prime Minister of Australia.
While writing his first book, The Alternative, Burton farmed outside Canberra and in 1960 was awarded a fellowship at the Australian National University. Two years later the Rockefeller Foundation awarded him a grant to study neutralism in Africa and Asia. In 1963, while a Reader in International Relations at University College University of London, he established the Centre for the Analysis of Conflict. He then went on to hold fellowships at numerous universities while living in Canberra.
In introducing Burton as a guest on Radio National, Phillip Adams said; "John Burton was probably the most controversial and visionary public servant of the 20th Century. Branded a pink eminence of the Labor Party by conservative critics, he was clearly one of the most important intellectuals and policy-makers associated with the Curtin Labor Government of the 1940s. As a close associate of 'Doc' Evatt and head of the department of External Affairs (now Foreign Affairs) he did more to shape Australian foreign policy towards Asia and the Pacific than any other person before or since."