State Department
In September 1942, she joined the Department of State, where she worked, aside from a short stint at the Department of Commerce, for almost twenty years, beginning as an Economic Officer in the Division of Postwar Planning.
During her first three years at the State Department, Dulles was involved in post-war economic planning. She helped determine the U.S. position on international financial cooperation and participated in the Bretton Woods Conference of 1944 at which the International Monetary Fund and the International Bank for Reconstruction and Development were established. After the end of World War II, in the spring of 1945 she went to Europe, where she became involved in the reconstruction of the Austrian economy as the U.S. Financial Attaché in Austria.
In 1949, Eleanor transferred to the German Austrian Division at the State Department, where she took an active interest in the affairs of Berlin and became a member of the informal 'Berlin Lobby' in the United States.
She worked for the Commerce Department for several months in 1951–1952, and then returned to the State Department Office of German Affairs shortly before her brother John Foster Dulles became Secretary of State. She successfully resisted his attempts to remove her from her position.
She made many trips to Berlin and was involved in planning the construction of the Berlin Medical Center. The Berlin Congress Hall, the U.S. contribution to the International Building Exhibition was nicknamed the Dulleseum (Dulles plus Museum) for the role of Eleanor and her brother John Foster in its financing and construction. Later, she was hailed as "the Mother of Berlin" for helping to revitalize Berlin's economy and culture during the 1950s.
In 1958, she described the working environment at the State Department:
This place is a real man's world if ever there was one. It's riddled with prejudices. If you are a woman in Government service you just have to work 10 times as hard–and even then it takes much skill to paddle around the various taboos. But it is fun to see how far you can get in spite of being a woman.
In 1959, Dulles transferred from the German Desk to the Bureau of Intelligence and Research, where she became involved in a study of economic conditions in underdeveloped countries. As part of the study she traveled extensively in Africa, Latin America and South Asia.
Secretary of State Dean Rusk requested her resignation on September 21, 1961, at the insistence of the Kennedy Administration following the April Bay of Pigs Invasion, a foreign relations disaster for the U.S. that her brother Allen had overseen as head of the CIA. She resigned in January 1962.