The Winnipeg Art Gallery has had a long and continuous commitment to the collection, research, exhibition, and publication of art by Canadian Inuit.

The Gallery began collecting Inuit art in the 1950s, when it was a new art form. In 1960 the Gallery was definitively set on a course of collecting Inuit artworks with the acquisition of a collection of 130 sculptures from George Swinton. Over the years, the Gallery's Inuit art collection has grown to its present size of close to 11,000 works largely through the donation or purchase of large collections. Each collection had been built carefully over time, and each had a particular focus. The enormous 4,000-piece Jerry Twomey Collection, received in 1971, was encyclopedic in scope, but others, such as that of Ian Lindsay, filled in focused areas of strength. For Lindsay, it was the early period, 1949 to 1955. Later collections amassed by George Swinton and Faye and Bert Settler highlighted the art and artists of the Kivalliq region. Other important sculpture collections received over the years have come from Bessie Bulman, Edith Prudence Hockin, Peter Millard, and The Hudson's Bay Collection. In 2007 the Gallery’s collection was again strengthened by a donation of 246 Inuit sculptures donated by Dr. Harry Winrob.

The Gallery’s graphics collection was significantly augmented in 1989 when1,400 prints and drawings were donated by Indian and Northern Affairs, Canada. In 1990, a donation of 626 prints was made by the Holman Eskimo Co-operative. In 1979 and 1982, fund-raising drives allowed the purchase from Sanavik Co-operative in Baker Lake of 882 print-drawings. The Gallery’s collection of works on paper currently numbers 3,800.

The first significant exhibition of Inuit art was organized by the WAG in 1964. Since 1972  there has been a full-time curator for this collection. To date, over 140 exhibitions of Inuit art have been organized by the Gallery and 38 catalogues have been published, providing much research in this field.