The roots of the collection reach back to the 1939 Stills Photography Division of the National Film Board of Canada and it did not have a permanent home until it moved to its purpose-built site at 1 Rideau Canal. The building, which was opened on May 7, 1992, was designed by architect Michael Lundhom, who adapted an old railway tunnel running alongside the Chateau Laurier. The glass and concrete entrance from the street, reminiscent of the colonnade leading into the National Gallery, lead patrons down to the main part of the museum which was located below street level.
On March 29, 2009 it was announced that the CMCP, which had been closed temporarily in 2006 due to a leak, would be permanently closed for conversion to committee rooms. Its collections and program of exhibitions have since been absorbed by the National Gallery of Canada. A campaign to maintain the CMCP at its purpose-built site was unsuccessful. The exhibitions are now showcased at the National Gallery of Canada.