Toelken began his teaching career at the University of Oregon in 1966. During nearly twenty years at the University, Toelken would serve as director for both Folklore and Ethnic Studies and also the Randall V. Mills Archives of Northwest Folklore. Toelken returned to Utah State in 1985: there he would serve as the director of the Folklore Program and co-director of the Fife Folklore Conference.
Toelken was known for his research into Navajo folklore, namely with the Yellowman family. Decades later, Toelken destroyed most of the physical records originating from his work with the Yellowman family, choosing to leave a set of cassette tapes with members of the family, not within an archive.
Over the course of his career, Toelken was president of the American Folklore Society from 1977 to 1978, and edited the Journal of American Folklore and Western Folklore. The American Folklore Society granted Toelken fellowship in 1981. He received four of the association's major awards: the Américo Paredes Prize and the Chicago Folklore Prize, both in 2007, followed by the Kenneth Goldstein Award for Lifetime Academic Leadership and the Lifetime Scholarly Achievement Award, in 2011 and 2016, respectively.
Toelken also served on the boards of a number of organisations, including the American Folklife Center of the Library of Congress, the National Endowment for the Arts Folklife Program, the Western Folklife Center, Utah Arts Council, and the International Ballad Commission.
Toelken, J. Barre (April 1959). "The Ballad of the 'Mountain Meadows Massacre'". Western Folklore. 18 (2): 169–172. doi:10.2307/1496486. JSTOR 1496486.
Toelken, Barre (1976). "The 'Pretty Languages' of Yellowman: Genre, Mode, and Texture in Navaho Coyote Narratives". Folklore Genres. pp. 145–170. doi:10.7560/724150-010. ISBN 978-0-292-73509-5. S2CID 192956069.