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The Original Headquarters Building was designed in the mid-1950s by the New York firm of Harrison and Abramovitz, designers of the UN building. Located about eight miles from downtown Washington, the grounds were envisioned by then Director of Central Intelligence, Allen W. Dulles, as an environment similar to a college campus.

The New Headquarters Building was designed in the early 1980s by the Detroit architectural and engineering firm of Smith, Hinchman & Grylls. The new building is joined to the west facade of the original building and includes two six-story office towers connected by a four-story core area. It is a steel and glass structure as compared to the precast concrete construction of the original building.

The cornerstone of the original building was laid on 3 November 1959, and construction was completed in November 1963. Construction of the new building began in May 1984. The cornerstone was laid by the then Vice President of the United States, George Bush, on 1 November 1985. Occupancy of the new building began in June 1988, and it was essentially completed and occupied in March 1991.

The original building consists of 1,400,000 square feet, and the new building contains 1,100,000 square feet of space. Buildings and grounds comprise 258 acres.