Szarkowski earned a BS in 1948 from the University of Wisconsin, Madison. He also received honorary degrees from the Philadelphia College of Art (1972) and Minneapolis College of Art and Design (1974).
Since 1962 Szarkowski was director of the Photography Department of the Museum of Modern Art in New York City. Previously he taught at the Albright Art School of the University of Buffalo, New York (1951-53), taught photography at the University of Minnesota, Minneapolis, in 1950 and worked as a photographer at the Walker Art Center in Minneapolis (1948-51).
Swarkowski spent almost three decades at the MOMA. During this time, he was responsible for bringing attention to some of the greatest photographers of our time. It was Szarkowski who first presented the brilliance of Diane Arbus, Lee Friedlander and Garry Winogrand in a joint exhibit which presented photographs from all three icons. At the time it was considered a groundbreaking exhibit, due to the content and appearance of the photographs. This was the first time photos were exhibited which mimicked snapshots in their casual style and appearance.