In 1941, Brantford Catholic High School opened in the basement of St. Ann's Elementary School with just one Grade 9 class. A new class was added each year until 1951 when the school moved to a former residence on Duffrin Ave. From 1951 to 1978, the priests of the Congregation of the Resurrection acted as the principals. In 1959, the schools name changed to St. John's College. In the 1970-71 school year, St. John's College absorbed with Providence College at the present day Paris Road location. In the 1980s, the student population had grown so much that several expansions were added to the building. A new cafeteria, triple gym, teacher lounge, and 13 classrooms were constructed with help from community fundraising. In 1989, more additions were made with the addition of the current main entrance, 9 classrooms, administrative offices, the 'cafetorium', health center and guidance center. In 1991, enrolment exceeded 1700 students. This necessitated the opening of Assumption College in September, 1992, as well as Holy Trinity Catholic High School in Simcoe, Ontario in 2001.
The team name for all St. John's teams is the St. John's Green Eagles. A few of the Eagles teams throughout the year include basketball, soccer, cheerleading, rugby, volleyball, football, baseball, softball, track and field, golf, wrestling, badminton, curling, fly fishing and tennis.
St. John's College is steeped in the arts, particularly Drama and Music. The music program is very well respected and has received numerous honours, including gold standing in the regional and national MusicFest competitions. The Drama department is known for its ambitious major productions, including Cats, Fame, Little Shop of Horrors, Our Town, Godspell, Fame, Into the Woods and Evita. For a short while, St. John's major musical productions of Jesus Christ Superstar (1995), Joseph and the Amazing Technicolor Dreamcoat (1996), and Peter Pan (1998), were produced at the Brantford Sanderson Centre for the Performing Arts. The 1984 musical Footloose will be performed during the 2008-2009 school year.
During the production of Joseph, the Saturday night performance was stopped in the middle of the "Close Every Door" scene due to a bomb threat, which was later attributed to a student at the school, who was arrested and charged. EVITA was presented in 2008 at the Sanderson Centre from May 28th - 31. Also notable is the school's yearly participation in the Sears Drama Festival, which has brought the department several awards of excellence.