[3] With a strong Anglican affiliation,[4] St John's College was officially opened by the newly arrived Bishop Robert Machray on 1 November 1866.

[5][6][7] The roots of the college, however, lie in the early years of the Red River Colony, where it served as a school for the settlers.

[4][5] In 1882, planning began of a new building for the college at a 4-acre lot on the west side of Winnipeg's Main Street at Church Avenue.

[10] Graduate training based on the German-inspired American model of specialized course work and the completion of a research thesis was introduced.

[4] In 1912, a 3-storey brick-&-stone structure was built on Church Avenue in Winnipeg to provide additional classroom and residential space for the nearby St. John's College.

On the main level were 3 classrooms, library, ladies’ parlour, and cloakroom, Master's room, Warden's office, and 4 bedrooms.

[11] The college moved to the University of Manitoba's Fort Garry campus in 1958, with dormitories for men and women to the east, teaching and administration to the west, and the chapel to the north.

[14] While having its own Council and Assembly, in all academic matters other than the Theology program, the college is subject to the regulations of the University of Manitoba Senate.