Debwewin, which means Truth, features contemporary First Nations, Metis and Inuit artwork from the TDSB's vast collection which includes work by prominent indigenous artists such as Norval Morriseau.
The inaugural exhibition was curated by Elder Dr. Duke Redbird.
"We're living in a time in Canada where great transitions are taking place and the old style of doing things is evolving," Redbird said in an interview.
"The past needs to be in place. There were sad chapters in the education of native people in Canada and that system was part of a colonial past. We are decolonizing the future."
John Chasty, a TDSB superintendent told CBC News, that the exhibit is "a step toward increasing respectful and positive relationships with First Nations and Metis communities.
"Our education system is part of the residential schools legacy and we need to bring our students and staff to that understanding," he said.
"It's important our students see things from a wider lens so we can move forward so nothing like that ever happens again."
The TDSB Museum is the largest public education collection in Canada, containing over one million objects including archaeological objects, decorative arts and paintings, prints, sculpture and drawings.
Chasty says students who pass through the museum will learn about the history of Toronto, art, and the First Nations and Metis communities.
"It all ties in with what they're learning in the classroom," he said.