He served as DCI and director of the CIG and the CIA from May 1, 1947, to October 7, 1950, and, after his retirement from the United States Navy, was a member of the board of governors of National Investigations Committee On Aerial Phenomena (NICAP) from 1957 to 1962.

After the war, then-Captain Hillenkoetter commanded the USS Missouri in 1946 before returning to his pre-war posting as naval attaché in Paris before becoming head of the Central Intelligence Group (CIG) in May 1947.

Under the National Security Act of 1947 he was nominated and confirmed by the U.S. Senate as DCI, now in charge of the newly established Central Intelligence Agency (December 1947).

"[3] Hillenkoetter was called before the Joint Committee on Atomic Energy (JCAE) to explain how the CIA not only failed to predict the test, but also how they did not even detect it after it occurred.

DCI Hillenkoetter convened an ad hoc group to prepare estimates of likely communist behavior on the Korean peninsula; it worked well enough that his successor institutionalized it.

Nebraska Congressman Howard Buffett alleged that Hillenkoetter's classified testimony before the Senate Armed Services Committee "established American responsibility for the Korean outbreak," and sought to have it declassified until his death in 1964.

[17] Perhaps Hillenkoetter's best-known statement on the subject was in 1960 in a letter to Congress, as reported in The New York Times: "Behind the scenes, high-ranking Air Force officers are soberly concerned about UFOs.

[19][20] Actor Leon Russom portrayed Hillenkoetter in an episode of Dark Skies, a 1996 television series presenting a story based conspiracies related to UFOs.