Upon completing the museum course in 1934, Rathbone's first job was as a lecturer in the education department of the Detroit Institute of Arts. In 1936 he was appointed curator of Alger House, a branch museum in Grosse Point, Michigan, where he lived with DIA director William Valentiner. In 1939 he assisted Valentiner in organizing the Masterpieces of Art exhibition at the World's Fair in New York. In 1940 Rathbone was appointed director of the St. Louis Art Museum (then the City Art Museum). At age 29, he was the youngest museum director in America. From 1943-45 he served in the U.S. Navy in Washington D.C. as head of combat artists, and in New Caledonia as an officer. Upon returning from New Caledonia he married Euretta de Cosson, a British ski champion, on February 10, 1945. Three children were born to the Rathbones in St. Louis: Peter (1946), Eliza (1948), and Belinda (1950). Rathbone also was instrumental in helping the German artist Max Beckmann move to America after the war by securing him a teaching position at Washington University, and organized his first major retrospective in the USA at the St. Louis Museum. He was a champion of modern art, and along with Joseph Pulitzer Jr., and Morton May, stimulated many other collectors of modern art in St. Louis.