Finletter practiced law in New York until he began his government service in 1941, as a special assistant to Secretary of State Cordell Hull on international economic affairs.

He returned back to public service July 18, 1947, when President Harry S. Truman established a temporary, five-man commission that inquired into all phases of aviation and drafted the national air policy report.

President Truman appointed Finletter as the second Secretary of the Air Force succeeding Stuart Symington on April 24, 1950, in which office he served until January 20, 1953.

In 1965, following his term as Ambassador to NATO, he retired from government service and returned to his law practice with the firm of Coudert Brothers, in New York City.

In January 1967, he approached Senator Eugene McCarthy to see if he was interested in challenging Lyndon Johnson for the 1968 Democratic nomination for president, on the issue of the Vietnam War.