One of his professors at St. Michael's was Lester B. Pearson, the future Prime Minister who encouraged Flahiff to follow a career in diplomacy.
Basil's Seminary in Toronto, Flahiff was ordained to the priesthood by Archbishop Neil McNeil on 17 August 1930.
Upon his return to Canada, Flahiff taught history and art at the Pontifical Institute of Medieval Studies from 1935 to 1954.
During that time, he also served as a professor of history at the University of Toronto (1940–1954) and Secretary of the Institute of Mediaeval Studies (1943–1951).
Flahiff was one of the Council Fathers at Vatican II and played a key role in the writing of several Conciliar documents.