[3] The DNI was given further responsibility for the entire IC's whistleblowing and source protection by President Barack Obama via Presidential Policy Directive 19 on October 10, 2012.

Senators Dianne Feinstein, Jay Rockefeller and Bob Graham introduced S. 2645 on June 19, 2002, to create the position of Director of National Intelligence.

After considerable debate on the scope of the DNI's powers and authorities, the United States Congress passed the Intelligence Reform and Terrorism Prevention Act of 2004 by votes of 336–75 in the House of Representatives, and 89–2 in the Senate.

Critics say compromises during the bill's crafting led to the establishment of a DNI whose powers are too weak to adequately lead, manage and improve the performance of the intelligence community.

The first director of national intelligence was former U.S. ambassador to Iraq John Negroponte who was appointed on February 17, 2005, by President George W. Bush, subject to confirmation by the U.S. Senate.

On January 29, 2009, retired Navy admiral Dennis C. Blair became the third DNI on after being nominated by newly inaugurated President Barack Obama.

[9] On July 20, 2010, President Barack Obama nominated retired Air Force lieutenant general James Clapper as the fourth DNI.

On November 13, 2024, President-elect Donald Trump announced his intention to nominate Army Reserve Lieutenant Colonel Tulsi Gabbard for Director of National Intelligence upon returning to the presidency in January 2025.

These plans include a series of initiatives designed to build the foundation for increased cooperation and reform of the U.S. Intelligence Community.

The ODNI's goal is to effectively integrate foreign, military and domestic intelligence in defense of the homeland and of United States interests abroad.

On March 23, 2007, DNI Mike McConnell announced organizational changes, which included: The ODNI continued to evolve under succeeding directors, culminating in an organization focused on intelligence integration across the community.