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John Bolton was named Trump’s third national security adviser in April 2018 after the departure of Army Gen. H.R. McMaster.SERGEI GAPON/AFP/Getty Images

U.S. President Donald Trump on Tuesday abruptly forced out John Bolton, his hawkish national-security adviser with whom he had strong disagreements on Iran, Afghanistan and a cascade of other global challenges.

The sudden shakeup marked the latest departure of a prominent voice of dissent from the President’s inner circle, as Mr. Trump has grown less accepting of advice contrary to his instincts. It also comes at a trying moment for Mr. Trump on the world stage, weeks ahead of the United Nations General Assembly and as the President faces pressing decisions on difficult foreign-policy issues.

Tensions between Mr. Bolton, Mr. Trump’s third national-security adviser, and other officials have flared in recent months over influence in the President’s orbit and how to manage his desire to negotiate with some of the world’s most unsavoury actors. Since joining the administration in the spring of last year, Mr. Bolton has espoused skepticism about the President’s whirlwind rapprochement with North Korea, and recently has become a vocal internal critic of potential talks between Mr. Trump and leaders of Iran and Afghanistan’s Taliban.

Mr. Bolton also broke with Mr. Trump with his vocal condemnation of Russia’s global aggressions, and last year, he masterminded a quiet campaign inside the administration and with allies abroad to persuade Mr. Trump to keep U.S. forces in Syria to counter the remnants of the Islamic State and Iranian influence in the region. Mr. Bolton’s manoeuvring at the time contrasted with former secretary of defence Jim Mattis’s decision to instead resign over Mr. Trump’s December withdrawal announcement, which has been effectively reversed.

On Twitter on Tuesday, Mr. Trump and Mr. Bolton offered opposing accounts on the adviser’s less-than-friendly departure, final shots for what had been a fractious relationship almost from the start.

Mr. Trump tweeted that he told Mr. Bolton on Monday night his services were no longer needed at the White House and Mr. Bolton submitted his resignation on Tuesday morning. Mr. Bolton responded in a tweet of his own that he offered to resign on Monday “and President Trump said, ‘Let’s talk about it tomorrow.'"

Mr. Trump explained that he had “disagreed strongly” with many of Mr. Bolton’s suggestions as national-security adviser, “as did others in the administration.”

Bolton’s letter of resignation, dated Tuesday, was only two sentences long. He wrote: “Dear Mr. President, I hereby resign, effective immediately, as assistant to the president for national security affairs. Thank you for having afforded me this opportunity to serve our country.” He signed the letter “Sincerely, John R. Bolton.”

South Carolina Senator Lindsey Graham, who had been travelling with Mr. Trump on Monday, said reports of Mr. Bolton’s opposition to a now-scrapped weekend meeting with the Taliban at Camp David was a “bridge too far” for Mr. Trump.

And one Republican familiar with the disagreements between Mr. Trump and Mr. Bolton said the adviser’s opposition to a possible meeting between Mr. Trump and Iranian President Hassan Rouhani was a precipitating factor. French President Emmanuel Macron has been trying to broker such a meeting, possibly on the sidelines of the UN General Assembly, in hopes of salvaging the international Iran nuclear deal from which Mr. Trump withdrew.

“There were many times that Ambassador Bolton and I disagreed. That’s to be sure,” Secretary of State Mike Pompeo said on Tuesday. He added that Mr. Trump has been clear that he is willing to meet with Mr. Rouhani “with no preconditions.”

Treasury Secretary Steven Mnuchin, who appeared with Mr. Pompeo at the White House, volunteered: “The President’s view of the Iraq war and Ambassador Bolton’s was very different.”

A former Bush administration official, Mr. Bolton has championed hawkish foreign-policy views dating back to the Reagan administration and became a household name over his vociferous support for the Iraq war as the U.S. ambassador to the UN under George W. Bush. Mr. Trump initially supported the 2003 U.S. invasion, but subsequently became a vocal critic.

The Iranian government hailed Mr. Bolton’s departure, and spokesman Ali Rabiei said it might pave the way for warmer relations. “By dismissal of the biggest supporter of war and economic terrorism, the White House will face less barrier to understand realities of Iran,” he said in a tweet. Tehran calls the U.S. sanctions on Iran “economic terrorism.”

Mr. Pompeo said, “I don’t think any leader around the world should make any assumption that because some one of us departs that President Trump’s foreign policy will change in a material way.”

Mr. Bolton’s well-known foreign-policy views and harsh rhetoric for U.S. foes had turned him into a convenient boogeyman for the likes of North Korea and Iran, which have assailed him in the media.

His ouster came as a surprise to many in the White House. Just an hour before Mr. Trump’s tweet, the press office announced that Mr. Bolton would join Mr. Pompeo and Mr. Mnuchin in a briefing on new Iranian sanctions. He did not.

As pressure has mounted amid global troubles and signs of an economic slowdown at home, Mr. Trump has increasingly favoured aides who are willing to defend him on television. Mr. Bolton was tentatively booked to appear on a pair of Sunday talk shows in late August but backed out, saying he was not comfortable with some of the administration’s plans, and that drew the President’s ire, according to a White House official not authorized to discuss private conversations

Mr. Bolton and his national-security council staff were also viewed warily by some in the White House who viewed them as more attuned to their own agendas than the President’s – and some administration aides have accused Mr. Bolton’s staff of being behind leaks of information embarrassing to Mr. Trump.

He was always an unlikely pick to be Mr. Trump’s third national-security adviser, with a world view seemingly ill-fit to the President’s isolationist “America First” pronouncements. He briefly considered running for president in 2016, in part to make the case against the isolationism that Mr. Trump would come to embody.

Still, Mr. Trump had admired Mr. Bolton for years, praising him on Twitter as far back as 2014. Mr. Trump had told allies he thought Mr. Bolton was “a killer” on television.

Defending Mr. Bolton after Tuesday’s announcement, a person close to him said they had been authorized to say one thing – that since he had been national-security adviser, there had been no “bad deals” on Iran, North Korea, Russia and Syria. The person, who did not divulge who had given the authorization, was not allowed to discuss the issue by name and spoke only on condition of anonymity.

When asked to respond to the person’s comment, White House press secretary Stephanie Grisham smiled and told reporters: “Sounds like just somebody trying to protect him.”

Democratic Senator Chris Murphy said the turnover in the President’s foreign-policy team was a cause for worry.

“John Bolton was the wrong choice and the silver lining to this instability is that there will be fewer people whispering war chants in the president’s ear,” Mr. Murphy said. “But no one of any quality is going to take a job in the nation’s national-security cabinet so long as everyone’s head is permanently hovering slightly above the chopping block.”

But Utah Senator Mitt Romney, the GOP’s 2012 nominee for president, bemoaned Mr. Bolton’s ouster, calling it “an enormous loss for the country and for the administration.”

He added that “in decision making you want people who disagree and who offer a very different perspective.”

White House spokesman Hogan Gidley said Charles Kupperman, the deputy national-security adviser and a former Reagan administration official and defence contracting executive, would fill Mr. Bolton’s role on an acting basis. Mr. Trump said he would name a replacement for Mr. Bolton next week.

Mr. Bolton was named to the post in March, 2018, after the departure of Army General H.R. McMaster.

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