The collection, worth at least a million dollars, contains 110 pieces in total. Twelve of the pieces are by A. Y. Jackson, a member of the renowned Group of Seven.
Other artists include Douglas Lawley, the former principal of Westmount High School, Anne Savage and Thoreau MacDonald.
The foundation entrusted with the collection said it wants to expose the art to the public.
The curator, Angelo Komatsoulis, said most of the paintings have been hanging in the school board's building.
The cost of insurance for the art pieces was also costing the foundation too much money.
"We did not yank the paintings off the wall. We approached the school board, we advised them of what direction we were heading. We were applauded for that, and then we proceeded to carry out our recommendation," he said
Julien Feldman, a school board commissioner, disagrees with the sale. He said the decision to auction off the collection should have been made with input from the public.
"This collection is the essence of the Anglo community and this discussion needs to take place in the open light, not in the smoky back rooms of the school board," he said.
Feldman said there are already scholarships in place and that selling to private collectors is irresponsible.
"To simply scatter it to the four winds, to disperse it via internet auction, is a scandal, frankly," he said.
The Heffel Art Auction in Vancouver will receive 35 paintings to be sold in the spring, another 25 will go to an online auction.
Some engravings on the history of Quebec and paintings of First World War will be donated to a museum.
The school board plans to keep some of the pieces for its offices.
Parents, school alumni and the artists themselves donated most of the pieces to the board.