In 1981, at the age of 23, Crumpton became the youngest trainee in his class at the CIA. He began his career at the CIA in the Africa division in Liberia in the 1980s. In 1998-99 he served as deputy chief in the FBI’s International Terrorism Operations Section, while on loan from CIA. In 1998 he investigated the al Qaeda bombings of the US embassies in Kenya and Tanzania and the 2000 attack of the USS Cole off the coast of Yemen. He was involved with Afghanistan until 2002 when he moved on to calmer assignments. He was the deputy director of the Counter-Terrorism Center from 1999 to 2001, and head of one of the agency's most secret divisions, the National Resources Division, from 2003 to 2005. As head of the National Resources Division he hired current CIA Director Gina Haspel as his deputy. He also was the head of the US covert response in Afghanistan to the September 11, 2001 attack, masterminding the 90-day overthrow of the Taliban. He worked for the CIA for a total of 24 years, served as State Department Coordinator for Counterterrorism with the rank of ambassador-at-large, and retired from government service in 2007.