In 1930, Lightner joined the United States Department of State. He was primarily active overseas, visiting a total of 18 countries in Latin America, Europe, Africa, and Asia until his retirement in 1970. He became Assistant Director for the Central European Division from 1945 to 1947; Deputy Director of the Central European Division from 1947 to 1948; Deputy Political Director for the High Commission in Frankfurt from 1949 to 1951. He then became charge d'affaires of the U.S. Embassy in South Korea (March 1, 1951 to February 1953), Consul General in Munich from 1953 to 1956, and Deputy Assistant Secretary of State for Public Affairs from May 14, 1956 to June 1959. Lightner also became assistant chief of the U.S. Mission in West Berlin from 1960 to May 1963. While stationed in Berlin, he witnessed the construction of the Berlin Wall in August 1961. Lightner had unrestricted access to all occupied areas within the city and occasionally entered East Berlin at the direction of the American government. Lightner was detained twice by East German border guards in October 1961.
In February 1962, he was present at the prisoner exchange at the Glienicke Bridge between American U-2 pilot Francis Gary Powers, who had been captured by KGB, and Rudolf Abel, a Soviet intelligence officer who had been captured by the FBI. After the incident, Lightner became an Ambassador to Libya from May 27, 1963 to June 30, 1965. He assisted in negotiations between the United States and the Libyan government regarding the Wheelus Air Base in Tripoli, which asked what they could use for their base.