[6] He also serves as a senior advisor to Ron Wahid, Chairman of Arcanum, a global strategic intelligence company and subsidiary of Magellan Investment Holdings.

According to journalist Alan Nairn, during his tenure as commander-in-chief of the U.S. Pacific Command, Blair disobeyed orders from civilians in the Clinton administration during the 1999 East Timorese crisis.

Amid growing international concern over violence against the independence movement in Indonesian-occupied East Timor, Blair was ordered to meet with General Wiranto, the commander of the Indonesian military, and to tell him to shut down the pro-Indonesia militia.

[22] During his confirmation hearing as Director of National Intelligence, Blair denied the accusations: "In our conversations with leaders of Indonesia, both military and civilian, we decried and said that the torture and killing that was being conducted by paramilitary groups and some military groups in East Timor had to stop"; "those who say that I was somehow carrying out my own policy or saying things that were not in accordance with American policy are just flat wrong".

[23] Blair was unanimously approved by the Senate Intelligence Committee,[24][25] his tenure lasting just fifteen months, at which point he was fired, reportedly for disobeying orders from President Obama.

Blair observed, "with all due respect to the Inspector General, I find it hard to understand how I could be criticized for violating conflict of interest standards when I didn't have any influence on the study".

[30] He served as president of the Institute for Defense Analyses (IDA) from 2003 to 2007, a U.S. government think tank in the Washington, D.C. area focused on national security.

[6] Blair is the co-head of the Commission on the Theft of American Intellectual Property along with former governor of Utah and Republican presidential candidate Jon Huntsman.

[33] Dennis C. Blair became the third Director of National Intelligence (DNI) on January 29, 2009, after being nominated by newly inaugurated President Barack Obama.

[36][37][38][39] In May 2009, Blair attempted to assert the DNI's role as the head of the Intelligence Community with a memo claiming authority to appoint CIA chiefs of station abroad.

[40] Blair's two predecessors, Mike McConnell and John Negroponte, were both unable to bring this role under the auspices of the DNI, the authority to appoint chiefs of station having been the province of the CIA since 1947.

[41] According to news reports, President Bush issued an executive order to give Blair his congressionally-mandated powers to force the CIA and other intelligence agencies to cooperate with his office.

On May 22, 2010, two days after the resignation was announced, U.S. officials leaked information to The New York Times stating that Blair's dismissal had been related to his continual pushing of a U.S.–French intelligence-sharing project "with other countries".

Blair and Bernard Bajolet, intelligence advisor to French President Nicolas Sarkozy, had commenced negotiations between October and December 2009 on the pact.

The treaty was to have been a legally binding reciprocal no-spying arrangement between France and the United States, whereby each country would take over operations for the other in their home-territory.

[59] Mr. Sarkozy was also in Washington for the 2010 Nuclear Security Summit from April 12–14, immediately prior to President Obama's rejection of the treaty produced by eight months of negotiations by Blair.

In an unusual response, the Palais de l'Elysee confirmed that such a treaty had been negotiated, adding that "we weren't the askers" in the deal, denying any French disappointment.

When it was discovered that the November 2009 Fort Hood shooting and the attempted bombing of Northwest Airlines Flight 253 a month later could have been prevented with better inter-agency intelligence sharing, Brennan and Panetta allegedly blamed Blair (which, according to Aid, was not justified), resulting in Obama's decision to replace him.