Richard Helms began working in intelligence during World War II and was director of the CIA from 1966 to 1973.
He was sacked by President Richard Nixon after refusing to help block an investigation into the Watergate scandal - which eventually brought Nixon down himself.
Helms was involved in some of the CIA's murkiest dealings, including plots to assassinate the Cuban leader, Fidel Castro, and the overthrow of President Salvador Allende of Chile.
Tributes
Richard Helms died at his Washington home late on Tuesday of unknown causes. He had been in declining health for some time.
Current CIA Director George Tenet paid tribute to him for steering "a bold and daring course" during his years at the head of the US intelligence agency.
"The men and women of American intelligence have lost a great teacher and a true friend," Mr Tenet said in a statement.
"Clear in thought, elegant in style, he represents to me the best of his generation and profession."
'Archetypal spymaster'
Richard Helms started his career as a journalist, and an early coup was an interview with Adolf Hitler.
He joined the US Navy during the war, then the Office of Strategic Services - the forerunner of the CIA - and stayed on after the war when the CIA was created.
He quickly rose through the ranks and was first made CIA Director by President Lyndon Johnson, later to be reappointed by President Nixon.
The BBC's Washington correspondent Nick Childs says Helms was in many ways the archetypal Cold War spymaster.
He led the CIA during both the Vietnam War and an unsuccessful attempt to overthrow the Chilean Government.
But when he resisted attempts by Nixon to involve the CIA in the Watergate scandal - which ultimately brought down his presidency - Helms was not reappointed to his post.
Instead he was made US ambassador to Iran.
Later, however, he was repeatedly called back to Washington to testify before congressional committees investigating the CIA's assassination schemes, its role in Chile and its alleged spy operations within the US.
Helms pleaded guilty and was given a suspended jail sentence - a troubling end to the career of a man who had devoted most of his working life to intelligence.
But despite his controversial career, his experience meant that his advice was still highly sought by his successors, our correspondent says.