Established in 1976 by the board of the Thunder Bay Historical Museum Society as a National Exhibition Centre, with funds from the federal government's Museum Assistance Program, the primary mandate of the Thunder Bay Art Gallery has been to research, collect, and exhibit the work of contemporary First Nations artists, and to host travelling exhibitions from other art galleries and museums. As of 2005 the board of directors approved a move to promote, encourage, and exhibit the works of local and regional artists.
The gallery was expanded in 1982. In 1986 it was officially named the Thunder Bay Art Gallery.
The gallery features three exhibition venues that change approximately every 6 weeks.