He returned to Shaw, working as an instructor of history (1935–39). He next taught at Dillard University (1939–1953) in New Orleans, Louisiana. There he became a full professor and also served as dean. His last appointment was as professor of history and chair of the department at Morgan State University, Baltimore, Maryland (1953–1974). At Morgan, Quarles reached near-legendary status as the long-time head of the History Department. He was a revered teacher and counselor, an intellectual and professional mentor for two generations of African-American scholars. Many of his books became required reading in the African-American history courses that were developed in American universities during the 1960s. This movement was inspired both by the civil rights movement and increasing scholarly interest in the history of minorities and women. After Quarles's official retirement in 1969, he was awarded professor "emeritus" status and kept teaching for several years.