Stackhouse received his higher education in Canada and the United States: after a year at Mount Carmel Bible School in Edmonton, he received a BA in history from Queen's University, an MA in church history and theology from Wheaton College, and a PhD from the University of Chicago with a dissertation supervised by Martin E. Marty.

Stackhouse began teaching at the International Teams School of World Missions and then Wheaton College, both in suburban Chicago, during his doctoral studies.

He wrote over 200 weekly web columns for "Context: Beyond the Headlines," a Canadian Christian public affairs television program, until 2020.

He writes occasionally for the Religion News Service, "Sightings" (produced at the University of Chicago Divinity School).

He has given expert testimony to the Canada Revenue Agency, the Manitoba Human Rights Commission, and the British Columbia Supreme Court.

In November 2023, Crandall University announced that it was terminating Stackhouse's employment following a six month independent investigation into allegations that he sexually harassed students.