After passing the Civil Service entrance exam, Poynton was recruited by the Department of Scientific and Industrial Research in 1927.
Two years later he was transferred to the Colonial Office, where his real interests lay, following his appointment as Assistant Principal.
[1][2] In 1943 he returned to the Colonial Office, serving Deputy Under-Secretary of State in charge of the Economic Division from 1948 to 1959.
He was also a member of the Conservative Commonwealth and Overseas Council's policy study group on the future of the Dependent Territories.
He was Treasurer of the Society for the Promotion of Roman Studies (1967–1976) and Director of the Overseas Branch of St John Ambulance (1968–1975).