After graduating from Yale and earning an MBA from Harvard Business School, Bekenstein helped found Bain Capital, which has grown from its inception in 1984 into a private alternative asset management firm with more than fifteen hundred employees in twenty-two offices on four continents. He stepped down from his co-chairman position on December 31, 2022. Bekenstein serves as a board member of several corporations, including Bombardier Recreational Products, Bright Horizons Family Solutions, Canada Goose, and Dollarama. Philanthropically, Bekenstein chairs the board of the Dana-Farber Cancer Institute and is a member of the boards of New Profit, the Environmental Defense Fund, and the Southern Poverty Law Center.
At Yale Bekenstein has served on the Corporation Committee on Investments and the School of Management Board of Advisors. He also served as an at-large member of the University Council, co-chair of the Yale Tomorrow Campaign, and a member of the Yale Development Council. He was named a successor trustee in 2013 and senior trustee in 2021.