Born in Scarsdale, New York, Huntington grew up with his mother and siblings in Princeton, New Jersey, graduating from Princeton Country Day, the Taft School in Connecticut, and Princeton University, where he studied architecture. Huntington earned a PhD from Yale University in art history, writing a dissertation on Frederic Church that is still cited for its significant contribution to Church scholarship, though never published. Huntington was teaching art history as an assistant professor at Smith College in Northampton, Massachusetts, when he led the campaign to Olana.
In June 1951, Huntington married Gertrude Enders, a fellow graduate student at Yale, in sociology, who was studying the Amish. She earned the first interdepartmental PhD awarded by Yale. David and Trudy Huntington had three children Caleb, Abby and Daniel. Soon after Olana was saved, Huntington was offered a position at the University of Michigan, where he was a beloved professor for almost 25 years. He suffered a fatal heart attack at age 67, leaving his loving family bereft, before he was able to tell the story of saving Olana, a project he was saving for his retirement.