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Dempsey worked as a journalist for the Edmonton Bulletin newspaper from 1948 to 1951 and then became a publicity writer for the Alberta Government from 1951 to 1956. In 1956, Dempsey was vice-president of the Edmonton-based Historical Society of Alberta and associate editor of the Alberta Historical Review, when he moved to Calgary to become archivist of the recently established Glenbow Museum. From 1956 until 1967, he worked as an archivist, and was a curator/director from 1967 to 1991. On his retirement Dempsey was made Chief Curator Emeritus.
Dempsey authored numerous articles and books, such as Crowfoot, Chief of the Blackfeet (1973), The Gentle Persuader: A Biography of James Gladstone, Indian Senator (1986), and Red Crow: Warrior Chief (1978), which focus on the culture and history of the First Nation peoples of Alberta. Dempsey's writing benefited not only from his work as an archivist but also from his access to the Blackfoot community through his marriage. Dempsey is credited with combining the oral history of native peoples with scholarly records to produce historical writing with a broad popular appeal.
Dempsey became editor of the Alberta Historical Review in 1958. From 1963 to 1967, Dempsey was also editor of the newsletter The Canadian Archivist which later became the journal of the Archives Section of the Canadian Historical Association. He also lectured on native studies and Alberta history at the University of Calgary.
Dempsey was the honorary secretary of the Indian Association of Alberta from 1959 to 1964 and was made an honorary chief of the Kainai Nation in 1967. Dempsey was presented with an honorary doctorate from the University of Calgary on May 30, 1974, after he gave the convocation address. On October 15, 1975 Dempsey was invested as a Member of the Order of Canada "for his contributions to the preservation of the cultural and development of interest in the history of the Plains Indians." In 1987, Dempsey was awarded the Certificate of Merit in Regional History by the Canadian Historical Association for his "distinguished career." On October 2, 2000, the Archives Society of Alberta paid tribute to Dempsey "for his lasting contributions" to the preservation of Alberta's heritage 
Dempsey was born in Edgerton, Alberta in 1929. In 1953 he married Pauline Gladstone, the daughter of Canadian SenatorJames Gladstone of the Kainai Blackfoot, with whom he had five children. In 1951 Dempsey began more than 40 years of correspondence and friendship with American ethnohistorian John Canfield Ewers when the two met while doing field research on the Blackfoot reservation in Montana.
Big Bear : The End of Freedom',, Saskatoon : Western Producer Prairie Books, 1986. ISBN 0-88833-208-4
Bibliography of the Blackfoot, (with Lindsay Moir), Native American bibliography series, no. 13. Metuchin, NJ: Scarecrow Press, 1989. ISBN 0-8108-2211-3
The Amazing Death of Calf Shirt and Other Blackfoot Stories : Three Hundred years of Blackfoot History, Norman : University of Oklahoma Press, 1996. ISBN 0-8061-2821-6
Tom Three Persons: Legend of an Indian Cowboy, Purich Publishing Ltd, Saskatoon SK, 1997. ISBN 1-895830-08-7
Charcoal's World: The True Story of a Canadian Indian's Last Stand, Canada Fifth House Publishers, Calgary, AB, 1998. ISBN 1-894004-20-5
Firewater: The Impact of the Whisky Trade on the Blackfoot Nation, Calgary: Fifth House Publishers, 2002. ISBN 1-894004-96-5
The Vengeful Wife and Other Blackfoot Stories, Norman: University Of Oklahoma Press, 2003. ISBN 0-8061-3550-6
The People of the Buffalo. The Plains Indians of North America. Essays in Honor of John C. Ewers, vol 1 & 2, co-editor with Colin F. Taylor, Tatanka Press, Wyk auf Foehr, 2003 (vol. 1), 2004 (vol, 2). ISBN 3-89510-101-X (vol.1) 3-89510-102-8 (vol.2)