Weiner argues the CIA has consistently failed its primary mission: informing the President about the world. He highlights major intelligence misses, including the Soviet atomic bomb (1949), the invasion of South Korea (1950), and the eventual collapse of the Soviet Union (1989).

The book posits that the agency became obsessed with "secret warfare" (coups, assassinations, and sabotage) at the expense of patient espionage and analysis.

The book received a polarized reception depending on the audience:

Tim Weiner's Legacy of Ashes: The History of the CIA is a National Book Award-winning chronicle that portrays the agency’s 60-year history as a series of profound failures that have jeopardized American national security.

The phrase "Legacy of Ashes" comes from President Dwight D. Eisenhower, who reportedly used it to describe the state of American intelligence near the end of his term.