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Further, President Gerald Ford, responding to protests about the intrusive activities of the CIA, set up a "Citizens' Commission" on January 4, 1975 to investigate whether it had spied on Americans inside the U.S. in violation of its charter. The CIA's charter was again enforced, with the FBI solely responsible for investigating U.S. citizens.

Repercussions from the Iran-Contra arms smuggling scandal included the creation of the Intelligence Authorization Act in 1991. It defined covert operations as secret missions in geopolitical areas where the U.S. is neither openly nor apparently engaged. This also required an authorizing chain of command, including an official, presidential finding report and the informing of the House and Senate Intelligence Committees, which, in emergencies, requires only "timely notification".

In 1988, President George H. W. Bush became the first former chief of the CIA to be elected President of the United States.

Previously, the Director of Central Intelligence (DCI) oversaw the Intelligence Community, serving as the president's principal intelligence advisor, additionally serving as head of the Central Intelligence Agency. The DCI's title now is "Director of the Central Intelligence Agency" (DCIA), serving as head of the CIA.

Currently, the Central Intelligence Agency reports to U.S. Congressional committees, but also answers directly to the President. The National Security Advisor is a permanent member of the cabinet, responsible for briefing the President with pertinent information collected by all U.S. intelligence agencies, including the National Security Agency, the Drug Enforcement Administration, et cetera; all fifteen Intelligence Community agencies are under the authority of the Director of National Intelligence.

Many of the post-Watergate restrictions upon the Central Intelligence Agency were lifted after the September 11, 2001 attacks on the World Trade Center in New York City and the The Pentagon. Some critics charge this violates the requirement in the U.S. Constitution that the federal budget be openly published. However, 52 years earlier, in 1949, Congress and President Harry Truman had approved arrangements that CIA and national intelligence funding could be hidden in the U.S federal budget.