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Memos from Sir Kim Darroch describing the Trump administration as inept were leaked to a British newspaper, infuriating the US President, who launched a Twitter attack on both the envoy and outgoing Prime Minister Theresa May, who had given Darroch her full support.
As a spat between the two close allies intensified, Trump said he would sever ties with the "very stupid" Darroch and called May "foolish".
The initial American response to the resignation took the long view. "The United States and the United Kingdom share a bond that is bigger than any individual, and we look forward to continuing that partnership," a State Department spokeswoman said.
Johnson, who could become Prime Minister later this month if grassroots Conservatives elect him as party leader, refused to back Darroch in a televised leadership debate on Tuesday night.
Darroch, who on Wednesday said his position had become untenable, had watched the TV debate, a diplomatic source told Reuters and another source familiar with the envoy's thinking said the former London mayor's comments "were a factor" in his decision to resign.
"He (Johnson) has basically thrown this fantastic diplomat under the bus to serve his own personal interests," said junior foreign minister Alan Duncan. "His sort of disregard for Sir Kim Darroch and his refusal to back him was, in my view, pretty contemptible."
However, at an event on Wednesday, Johnson told reporters that whoever leaked the memos should be "eviscerated".
'CLUMSY AND INEPT'
In confidential memos dating from 2017 to the present, Darroch had said reports of in-fighting in the White House were "mostly true". Last month, he described confusion within the administration over Trump's decision to call off a military strike on Iran.
"We don't really believe this Administration is going to become substantially more normal; less dysfunctional; less unpredictable; less faction-riven; less diplomatically clumsy and inept," the 65-year-old wrote in one cable.
It led to a scathing tirade from Trump.
"The wacky Ambassador that the UK foisted upon the United States is not someone we are thrilled with, a very stupid guy," he tweeted, describing Darroch as a "pompous fool".
Darroch had been due to step down at the end of the year.
"Since the leak of official documents from this Embassy there has been a great deal of speculation surrounding my position," he said in his resignation letter.
"The current situation is making it impossible for me to carry out my role as I would like."
An inquiry is under way into who leaked the memos, and why.
"Somebody has, for whatever malicious reasons, sought to either damage the UK-US relationship or indeed Sir Kim personally," British trade minister Liam Fox told reporters.
"I don't know what the motivations would be at this stage but it is very important that we find out who actually carried out this particularly damaging act."
Britain prides itself on its "special relationship" with its closest ally and Trump himself described it as "the greatest alliance the world has ever known" during a lavish state visit to Britain last month.
That relationship is of particular importance to London now, as it hopes to strike a major trade deal with Washington when Britain leaves the European Union.
Darroch, a career diplomat who was previously Britain's envoy to the EU, had been accused by some Brexit supporters of being biased towards the bloc.
Trump himself had previously suggested that Nigel Farage, now leader of the Brexit Party, would be a good choice as ambassador, irritating British officials.
Farage said this week he was not the right man for the job, but on Wednesday, after Darroch's resignation, tweeted: "The right decision, time (to) put in a non-Remainer who wants a trade deal with America."
May said the government did not share Darroch's views of the Trump administration, but that British ambassadors should have the freedom to give frank assessments, and that it was a matter of great regret that he had felt he had to quit.
During a campaign visit on Wednesday, Johnson, who was himself foreign minister until a year ago, called Darroch "a superb diplomat", adding that whoever leaked the documents had "done a grave disservice to our civil servants".
The main opposition Labour Party said Darroch had been bullied out by Trump and because of Johnson's "pathetic lickspittle response".
"It makes a laughing stock out of our government," said Emily Thornberry, Labour's foreign affairs spokeswoman.
"(Johnson) claims to regard Winston Churchill as his hero. But just imagine Churchill allowing this humiliating, servile, sycophantic indulgence of the American president's ego to go unchallenged."
The head of Britain's diplomatic service, Simon McDonald, said it was unprecedented for a head of state, friendly or hostile, to refuse to work with British ambassadors, who are generally professional diplomats, not political appointees.
The last time there was a problem with an envoy to Washington was in 1856, he said.
Johnson says he should be the one to replace May because his insistence on leaving the EU as scheduled on October 31, with or without a transition agreement, will spur the EU to give Britain a better deal than the one she secured in two years of talks but failed to get through parliament.