It was designed by architect Moshe Safdie, and opened its doors to the public on 19 October 1988.

[1] The previous buildings of the Banque de Paris and the Maison Estèbe, which were situated on Saint-Pierre street, were integrated in the museum's structure.

The institution also hosts Quartier des découvertes (Discovery Zone), geared towards children, and offers other services such as guided visits, a French America reference centre, shows, souvenir boutiques, a cafeteria, and a leisure room.

During the spring of 2021, The Globe and Mail published an article by journalist Kate Taylor about research concerning the museum's large collection of human remains.

This collection, on long-term loan from the provincial Ministry of Public Security, includes more than one hundred body parts—such as tattooed skin from a twenty-nine-year old homicide victim named Mildred Brown—taken from the bodies of murder victims by Dr. Wilfrid Derome during the early twentieth century.