The faculty's history is rooted in the numerous theological colleges in Montreal that became affiliated with the university during the nineteenth century. The creation of a joint board for the study of theology in 1912 allowed the colleges some autonomy in the provision of professional training for Christian ministry. This led to the creation of the Faculty of Divinity in 1948, which assumed the role of the joint board.
The faculty is located in the William and Henry Birks Building, at 3520 University, a Collegiate Gothic structure named in honour of Henry Birks and one of his sons.The building was built between 1929 and 1931 by Harold Fetherstonhaugh, a student of Percy Nobbs, for its original owners, the Joint Board of Theological Colleges. It was known by its original name, Divinity Hall, until 1972.