Elders, former students and young people spoke passionately of their own experiences, praying and singing during the dedication.
Some recalled the pain the schools caused multiple generations of Canada's aboriginal community and others spoke of the need to move forward from the mistakes of the past.
The artwork, which is now installed above the members' entrance to the House of Commons, was designed by Métis artist Christi Belcourt. A committee of aboriginal art experts and former students of the schools unanimously selected her design, unveiled last June.
The chosen design was translated into stained glass by Vision Art Glass Studio.
House of Commons Speaker Andrew Scheer accepted the new window on behalf of Canadians.
Aboriginal Affairs Minister John Duncan called the design a "profound and moving piece of art."
Belcourt called her work Giniigaaniimenaaning, which means "looking ahead" in an Ojibway language.
The year 2008 is featured at the top of the window — a reference to the Canadian government's official apology that year to survivors of Indian Residential Schools.
Duncan paid tribute to the design as not only a reminder of the schools' legacy, but also "a window to a future founded on reconciliation and respect."