Miller's tenure in the Trump administration began as Director of the National Counterterrorism Center, confirmed by voice vote in the United States Senate on August 6, 2020.

[2][3][4] President Donald Trump named Miller acting defense secretary after firing Mark Esper on November 9, 2020, six days after the 2020 presidential election.

[17] Miller attended Iowa City High School,[22] before earning a Bachelor of Arts degree in history from George Washington University in 1987.

He was part of the quick reaction force (QRF) after ODA 574 was hit by a Joint Direct Attack Munition (JDAM) in a friendly fire incident.

[30] Miller served in the civil service as an inspector for the assistant to the secretary of defense for intelligence oversight from late 2017 until he was detailed to the National Security Council in March 2018.

The top Republican on the House Armed Services Committee, Rep. Mac Thornberry, feared that U.S. adversaries would be emboldened by Trump's sudden withdrawals from conflict zones, and lame-duck purges of advisory boards.

[35] Miller's chief of staff as acting secretary of defense was Kash Patel, a former aide to Congressman Devin Nunes.

[36] Miller's first overseas trip occurred in the third week of November when he visited multiple military units in the Middle East and Africa to include a three-hour stopover in Mogadishu.

[38][39][40] Some were critical of the decision with one group calling it "11th hour of President Donald Trump's administration, risk serious harm to hard-fought counterterrorism gains and American safety.

With these recent moves, Miller appears to be disregarding important lessons about terrorists' resilience and the value of partnerships when conducting counterterrorism, while embracing a politically expedient but strategically nonsensical notion of 'ending forever wars' to appease the president during his final weeks in office.

"[41] They also pointed to the inconsistency in Miller's message where he claimed that the United States is "on the verge of defeating al-Qa'ida" and noted the need to avoid "our past strategic error of failing to see the fight through to the finish," while also making the audacious statement that "Now, it's time to come home.

[42][43][36] On January 3, 2021, all ten living former defense secretaries released an open letter in which they expressed concerns about a potential military coup to overturn the election results.

Miller testified that he told the president that Washington, D.C., Mayor Muriel Bowser had placed a request for unarmed personnel to reinforce local law enforcement.

[45] On January 5, Miller issued orders which prohibited deploying D.C. Guard members with weapons, helmets, body armor, or riot control agents without his personal approval.

[46] On January 5, Secretary of the Army Ryan McCarthy issued a memo placing limits on the District of Columbia National Guard.

[51] In a January 14, 2021, interview, Miller praised Russia's military capabilities, given their larger problems (e.g., declining population and single source of revenue) saying, "professionally I'm like, wow, they're doing pretty well, and they're using a lot of irregular warfare concepts, information, all this stuff, in a way that, you know, like .

[56] In 2023, Miller authored the chapter on the Department of Defense for the ninth edition of the Heritage Foundation's book Mandate for Leadership, which provides the policy agenda for Project 2025.