Washington CNN  — 

When Director of National Intelligence Dan Coats and his deputy Sue Gordon leave their offices for the last time on Thursday, it will mark a turning point for an administration that has already endured the highest level of senior staff turnover in history.

Both Coats, who took on the role of intelligence chief in 2017, and Gordon, who started as his deputy a few months later, have outlasted a slew of their national security colleagues who left the Trump administration at various points over the last two years.

This “is a defining day in the Trump administration’s national security structure – they have finally cleared out all the national security positions in terms of senior officials,” said David Priess, a former CIA official who delivered the president’s daily briefing in the administrations of Bill Clinton and George W. Bush.

“With all the twists and turns in the Trump administration and the national security establishment and intelligence community over the past two years, at least there has been stability in one way – the DNI and his principal deputy have quietly remained an island of steadiness,” Priess said. “As of August 15, that changes.”

Trump’s relationship with the intelligence community has been fraught from the very inception of his presidency, when the country’s most senior spies and security chiefs sat the newly minted leader down to brief him about Russian meddling in the 2016 presidential election and allegations that Moscow had material that could potentially compromise him.

Since taking office, Trump has repeatedly clashed with intelligence officials, including Coats, over their public comments acknowledging Russia not only interfered in 2016, but also poses a threat to future elections – an assessment that was reaffirmed by former special counsel Robert Mueller’s investigation, which the President often characterized as a “political witch hunt.”

Coats also drew Trump’s ire when he appeared to contradict him on various issues during a Senate hearing earlier this year. Still, lawmakers on both sides of the aisle have said that Coats’ dedication to speaking the “truth” was a quality they not only respected, but believe is a prerequisite for any nominee to replace him.

Similarly, Gordon was widely viewed, both within the intelligence community and among Congressional lawmakers, as an experienced official with the integrity and professionalism to tell the President facts he might not want to hear.

However, White House officials have told CNN that the President was never going to allow Gordon to assume the acting or permanent position due to her perceived ties to intelligence officials like former CIA Director John Brennan and even Coats.

When discussing his attempt to replace Coats with Republican Rep. John Ratcliffe of Texas on July 30, the President told reporters that the intelligence community needed “somebody like that that’s strong and can really rein it in. As you’ve all learned, the intelligence agencies have run amok. They’ve run amok.”

Coats’ and Gordon’s departures are “a story that combines two different issues that have become entangled with each other,” according to George Beebe, director of the Intelligence Project Center for a New National Interest.

One issue, he said, involves “the management and leadership of the intelligence community itself and the role it’s playing and should play in our national security system. The second is a domestic political story that has to do with Trump’s election, his presidency, his agenda for his presidency and the fact that there are an awful lot of people in Washington and in the country who are fundamentally opposed to the Trump presidency,” he said.

Beebe told CNN that it is difficult to understand the importance of Coats, Gordon and whoever the new leaders of the ODNI turn out to be, without getting into that domestic political story.

“The intelligence community is not supposed to be playing a political role in our tradition,” he added. “We’re not supposed to have a secret police … normally the impulse Americans have and Congress has and the media has is to want to place constraints on the intelligence community, to make sure they’re staying within the lines.”

‘Constrain the President’

“That dynamic has flipped now. People are seeing the intelligence community not as something that should be constrained, but something that should constrain the President,” Beebe said.

Until Trump picks a nominee, Joseph Maguire, former director of the National Counterterrorism Center, will serve as the acting Director of National Intelligence.

A US intelligence official told CNN that Maguire is well respected among career professionals, particularly due to his military background.

Maguire is also seen as an experienced hand at a time when the US faces a myriad of national security challenges.

Tensions with Iran are escalating in the Persian Gulf, North Korea continues to develop its weapons capabilities, arms control experts warn of a potential nuclear arms race with Russia and trade tensions with China are intensifying, while Trump is discussing a drawdown of forces in Afghanistan and Syria.

Trump left the door open to nominating Maguire for the full-time job last week, but his future remains uncertain.

Meanwhile, Gordon’s role will remain vacant, though Maguire can choose someone to perform those duties in the interim.

For both positions, the decision lies with Trump, but the White House’s list of candidates for the DNI role has only grown in recent weeks, with no indication that a nomination is coming soon.

And if Trump’s track record of dealing with national security vacancies is any indication, Maguire could serve in an acting capacity for a while.

Over the months that multiple geopolitical crises have been brewing, and since Trump took office, he has plowed through a Cabinet’s worth of national security professionals.

Cabinet churn

The President has run through two national security advisers – Michael Flynn and H.R. McMaster. There have been rumblings of his unhappiness with his most recent pick, John Bolton. Trump has summarily fired a secretary of state, Rex Tillerson, by tweet after undercutting the former ExxonMobile CEO for months.

Secretary of Defense Jim Mattis resigned, reportedly in frustration over Trump’s decision to pull out of Syria.

The President has churned through two Homeland Security secretaries, John Kelly and Kirstjen Nielson, and a National Security Agency director, Mike Rogers. He’s lost a deputy national security adviser, K.T. McFarland and an ambassador to the UN, Nikki Haley. Michael Pompeo, Trump’s former CIA director, has held on but moved over to helm the State Department.

Amid that churn, Coats and Gordon have been a steady, stabilizing influence, Priess said.

“The very fact that in this administration with the highest turnover in history, the people who are specifically designated to tell the truth to the President, whether he likes it or not, have remained in place, doing that day after day, means that by definition, they have been an island of stability,” Priess added.

While Trump’s decision to name Maguire as the acting replacement has appeared to be well received, he remains somewhat of an enigma despite his impressive military credentials and counterterrorism experience. Maguire is not widely considered to be part of the intelligence “establishment,” and sources close to him have told CNN that he has likely had limited interactions with the President.

But Maguire said that he has no problem speaking truth to power during the confirmation hearing for his job at the National Counterterrorism Center.

“I promise to tell the truth and to be able to represent the information and the hard analysis from the intelligence community professionals as accurately and as forthcoming as I possibly can, and I am more than willing to speak truth to power,” he told Democratic Sen. Mark Warner of Virginia, vice chairman of the Senate Intelligence Committee.

Warner again emphasized the importance of that quality in a statement last week.

“When I supported Admiral Maguire’s previous nomination, I made it clear I expected him to empower the intelligence professionals he led to do their important work free from political interference. Given the circumstances of his appointment as Acting DNI, it is more important than ever that Admiral Maguire stands by that commitment to speak truth to power,” he said.

“His success or failure in this position will be judged by the quality of work produced by the intelligence community, not by how those intelligence products make the President feel,” Warner added.

CORRECTION: This story has been updated to correctly reflect that Mike Rogers was the former director of the National Security Agency.

CNN’s Nicole Gaouette contributed to this report