John Agresto has taught at the University of Toronto, Kenyon College, Duke University, Wabash College, and the New School University. He was a scholar at the National Humanities Center in North Carolina and later served in senior positions at the National Endowment for the Humanities. He was president of St. John's College in Santa Fe for 11 years.

In 2003, Agresto went to Iraq as the Senior Advisor for Higher Education and Scientific Research for the Coalition Provisional Authority. Between 2007 and 2010, he occupied roles including academic dean, provost, and chancellor at the American University of Iraq. He has also been the Lilly Senior Research Fellow at Wabash College, scholar-in-residence at Hampden-Sydney College, and fellow at the James Madison Program in American Ideals and Institutions at Princeton University.

Agresto has authored five books and edited three others, including Rediscovering America; Mugged by Reality; The Supreme Court and Constitutional Democracy; The Humanist as Citizen; a cookbook; and a political/religious thriller under a pen name. His essays have appeared in the New York Times, Wall Street Journal, and Washington Post, among others.

Though recently retired as the probate judge of Santa Fe County, Agresto remains president of John Agresto & Associates, an educational consulting company.