After World War II until the creation of DIA, the three Military Departments collected, produced and distributed their intelligence for individual use. This turned out to be too duplicative, costly, and ineffective as each department provided their estimates to the Secretary of Defense or to other governmental agencies.

The Defense Reorganization Act of 1958 wanted to correct these deficiencies by assigning responsibility for Unified and Specified Command intelligence support. However, the intelligence responsibilities remained unclear, the coordination was poor and the first results were short of national reliability and focus. As a result of this poor organization, President Eisenhower appointed the Joint Study Group in 1960 to find better ways for organizing the nation's military intelligence activities.

Acting on the recommendations of the Joint Study Group, Secretary of Defense Robert S. McNamara advised the Joint Chiefs of Staff (JCS) of his decision to establish the Defense Intelligence Agency in February 1961. He assigned them with developing a concept plan that would integrate all the military intelligence of the DoD. The JCS completed this assignment by July, and published DoD Directive 5105.21, "Defense Intelligence Agency" on 1 August, effective 1 October 1961.

DIA reported to the Secretary of Defense through the JCS. It was a union of Defense intelligence and counterintelligence activities, and did not add administrative layering within the Defense intelligence community. The Agency's mission was the continuous task of collecting, processing, evaluating, analyzing, integrating, producing, and disseminating military intelligence for the DoD. Other objectives included more efficiently allocating scarce intelligence resources, more effectively managing all DoD intelligence activities, and eliminating redundancies in facilities, organizations, and tasks.

During the summer of 1961, as Cold War tensions flared over the Berlin Wall, Air Force Lieutenant General Joseph Carroll, soon to become DIA's first director, planned and organized this new agency. It began operations with a handful of employees in borrowed office space on 1 October 1961.

Following DIA's establishment, the Services transferred intelligence functions and resources to it on a time-phased basis to avoid rapidly degrading the overall effectiveness of defense intelligence. Specifically, DoD assigned DIA the mission of collecting, processing, evaluating, analyzing, integrating, producing, and disseminating military intelligence for the Department.

A year after its formation, the Agency faced its first major intelligence test during the superpower confrontation that developed after Soviet missiles were discovered at bases in Cuba.

In late 1962, DIA established the Defense Intelligence School (now the National Defense Intelligence College), and on 1 January 1963, it activated a new Production Center. Several Service elements were merged to form this production facility, which occupied the "A" and "B" Building at Arlington Hall Station, Virginia.

The Agency also added an Automated Data Processing (ADP) Center on 19 February, a Dissemination Center on 31 March, and a Scientific and Technical Intelligence Directorate on 30 April 1963. DIA assumed the staff support functions of the J-2, Joint Staff, on 1 July 1963. Two years later, on 1 July 1965, DIA accepted responsibility for the Defense Attaché System--the last function the Services transferred to DIA.

During these early years of DIA's existence, Agency attempts to establish itself as DoD's central military intelligence organization met with continuing Service opposition. At the same time, the Vietnam War severely tested the fledgling Agency's ability to produce accurate, timely intelligence. In particular, the war increased defense intelligence's involvement in efforts to account for American service members missing or captured in Southeast Asia.

DIA analysts focused during the 1960's on: China's detonation of an atomic bomb and the launching of its cultural revolution; increasing unrest among African nations; and, fighting in Cyprus, and Kashmir; and the missile gap between the US and the Soviets. In the late 1960's, crises that tested intelligence responsiveness included: the Tet offensive in Vietnam; the Six-Day War between Egypt and Israel; continuing troubles in Africa, particularly Nigeria; North Korea's seizure of the USS Pueblo; and the Soviet invasion of Czechoslovakia.

Since 9/11 DIA has been active in nuclear proliferation intelligence collection and analysis with particular interests in North Korea and Iran as well as counter-terrorism. DIA was also involved with the intelligence build-up to the invasion of Iraq in 2003 and was a subject in the Senate Report of Pre-war Intelligence on Iraq. The Defense Intelligence Agency has conflicted with the CIA in collection and analysis on the existence of WMDs in Iraq and has often represented the Pentagon in the CIA-DoD intelligence rivalry due to DIA's alleged clandestine HUMINT collection and often overlapping analysis products. Operational military intelligence has also been a focus, particularly in Iraq with insurgency threats and asymmetric warfare. Further, DIA is responsible for assessing the current and projected national security threats to the United States and presenting these assessments to the Senate Armed Services committee. Finally, DIA still actively maintains its responsibility for conventional strategic and operational military intelligence.