In a leadership debate, Johnson demurred when asked about Darroch's status and what it might be under a Johnson government. With Trump declaring that he would no longer do business with Darroch, and Johnson declining to give the ambassador stand-up backing, Darroch was left with no choice but to leave. His resignation only highlights the deterioration of the relationship between the two countries since Trump took office.
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Nigel Sheinwald, a former British ambassador to the United States, called Trump's treatment of Darroch "vindictive and undignified," adding that the President has repeatedly taken advantage of a government weakened by the Brexit stalemate.
"This would never have happened under any other presidency in modern times and it shows the strains in the UK-US relationship," he said.
Trump and May have had a stormy relationship from the start. British officials, including Darroch, worked hard to make certain she was the first foreign leader to visit Trump in the White House as a way to highlight tight US-British ties. British officials, including Darroch, carefully planned Trump's last two visits to the United Kingdom to minimise friction between the two principals and maximise the pomp and ceremony to emphasise the long-standing friendship between the countries.
On a personal level, however, Trump repeatedly denigrated May, primarily over Brexit, the referendum that called for the United Kingdom to leave the European Union. He has criticised her negotiating tactics with EU leaders, offered his own strategy as superior and undercut her whenever it suited him, including in the past few days as the Darroch controversy was unfolding.
His up-and-down relationship with May stands in contrast to that of recent past presidents, who have enjoyed strong bonds with their British counterparts. Ronald Reagan and Margaret Thatcher occasionally sparred but were united in their conservative visions and their views of the then-Soviet Union during the Cold War.
Bill Clinton and Tony Blair formed a partnership to advance centrist remakes of their political parties and tie their countries together. They were modernisers who brought their parties back to power and sought to spread the New Democrat and New Labour gospel elsewhere.
When America was attacked on September 11, 2001, Blair was the first foreign leader to speak with President George W. Bush by telephone, and he offered unwavering support to Britain's ally. Blair remained steadfast in his support of Bush's subsequent policies, including the invasion of Iraq in 2003, something that has tarnished the legacies of both leaders but especially Blair's back home in Britain.
Trump has followed a different script. He and the Brexiteers are cut from similar cloth - outsiders who tapped populist and anti-elite sentiment in their countries to upend and ultimately remake the politics on both sides of the Atlantic. Which is why he has been friendly with Nigel Farage, who led the pro-Leave forces during the Brexit referendum.
More importantly, over the course of his presidency, Trump has played nice to Johnson - and Johnson has responded in kind. On the eve of his visit to Britain a year ago, the President offered praise for Johnson as a possible future prime minister in an interview with a British newspaper, publication of which caused huge embarrassment for May. Even then, Johnson was angling to oust May.
Johnson, whose tenure as foreign secretary drew widespread criticism, will start on more solid ground with Trump than May has had. But will it continue? If he becomes prime minister, he will have to navigate a strategy for leaving the EU that eluded May. He has been equivocal during the campaign debates about just how he would do that.
May announced her decision to step down in June. After several elimination rounds of voting by Conservative members of Parliament, Johnson and Hunt emerged as the finalists. The winner will be chosen by rank-and-file Conservative Party members across Britain, with voting now underway. Balloting closes July 21, with the winner expected to be announced July 23.
If Johnson becomes leader and therefore the new prime minister, his selection of a new ambassador will be a telling indicator. Will he select someone political to appease Trump, or will he appoint a career Foreign Service officer, someone who will send a signal to his entire diplomatic corps that he believes in unvarnished private analysis, even while maintaining cordial relations with the administration.
There is no easy path, given the divisions in Britain today. Brexit has split the country in two, Leavers and Remainers. That division often overrides traditional left-right differences between the two major parties. Both Labour and Conservatives are split between their pro- and anti-Brexit factions, and the European elections at least showed greater support for the lesser parties, who had clear positions on Brexit, rather than the traditional major parties.
Britain has until the end of October to find a path out of the EU or face the prospect of a no-deal departure. Once out of the EU, Britain wants and needs a trade relationship with the United States. Johnson may believe he can strike that deal with Trump better than anyone else. Perhaps he is right, but it is placing a bet on the President that comes with substantial risk.
Darroch's resignation has forced a moment of reflection, a moment of reckoning, in the relationship between the longtime allies. The traditional ties - cooperation on defense and intelligence issues, cultural relations and all the rest - will continue apace. British and US government officials will do their work as they have tried to do it for years, cordially and professionally.
But with Trump in the White House and operating as no president has before - throwing his weight around to try to force other independent actors to do what he wants - and with Brexit still unresolved and now the major fault line in British politics, the relationship between the two countries faces a period of severe strain and possible remaking. Right now, Trump appears to have the upper hand in all this, and it will be left to the next leader of Britain to find that country's new equilibrium.