After graduation, John Flanders was employed as a junior architect in the London firm of the Architects Co-Partnership, where he worked on post-war schools and buildings for the Nigerian Ports Authority. In 1957 he joined the Ottawa firm of Hart Massey Architect, and later became a partner in Massey and Flanders Architects. This firm completed a number of commissions, including: buildings for Carleton University, mini-rail stations for Expo 67 in Montreal, the Faculty of Law building for the University of Toronto, The Sir John Carling Building for the federal government, and a number of private houses.
The Massey firm won a number of design awards, including two Massey Medals, and a Canadian Architect magazine Award of Excellence for Innis College designed for the University of Toronto that was never built. Massey and Flanders Architects closed their office in 1971, when their documents were donated to the National Archives.