Stackhouse began teaching at the International Teams School of World Missions and then Wheaton College, both in suburban Chicago, during his doctoral studies. His first full-time position was as an assistant professor of European history at Northwestern College in Orange City, Iowa (1987–90), where he chaired the department in his latter two years and won the college's teaching award. From there, he went to teach Modern Christianity (history, sociology, philosophy, and theology) in the Department of Religion at the University of Manitoba, in Winnipeg, Manitoba, Canada, rising to the rank of Professor in 1997 and receiving the university's top awards for research and for outreach to the community (via his newspaper column and other media appearances). One year later, he left for Regent College in Vancouver (1998–2015), where he served as the Sangwoo Youtong Chee Professor of Theology and Culture at Regent College, in the position formerly held by J. I. Packer.