As a Marine, Stockwell was a CIA paramilitary intelligence case officer in three wars: the Congo Crisis, the Vietnam War, and the Angolan War of Independence. His military rank is Major. Beginning his career in 1964, Stockwell spent six years in Africa, Chief of Base in the Katanga during the Bob Denard invasion in 1968, then Chief of Station in Bujumbura, Burundi in 1970, before being transferred to Vietnam to oversee intelligence operations in the Tay Ninh province and was awarded the CIA Medal of Merit for keeping his post open until the last days of the fall of Saigon in 1975.
In December 1976 he resigned from the CIA, citing deep concerns for the methods and results of CIA paramilitary operations in third world countries and testified before Congressional committees. Two years later, he wrote the exposé In Search of Enemies, about that experience and its broader implications. He claimed that the CIA was counterproductive to national security, and that its "secret wars" provided no benefit for the United States. The CIA, he stated, had singled out the MPLA to be an enemy in Angola despite the fact that the MPLA wanted relations with the United States and had not committed a single act of aggression against the United States. In 1978 he appeared on the popular American television program 60 Minutes, claiming that CIA Director William Colby and National Security Advisor Henry Kissinger had systematically lied to Congress about the CIA's operations.