His dramatic resignation followed those of Davis and his deputy Steve Banker overnight over May's plans to keep Britain economically close to the bloc. "At least half a dozen people made that point and the prime minister responded, too - what is good for the country is a Conservative government".
With less than nine months left until Britain is due to leave the bloc, May is sticking to her plan for a "business friendly" Brexit, facing down hard-line Brexit supporters in her Conservative Party who are livid over her plans to negotiate a "free-trade area for goods" with the EU.
He has criticised May over her response to terrorism and approach to Brexit, and infuriated many in Britain when he retweeted a far-right group.
He said Brexiteers need to accept that pursuing a hard Brexit would likely fail to clear the Commons, risk thousands of job losses and threaten peace in Northern Ireland.
"The Government now has a song to sing. The trouble is that I have practised the words over the weekend and find that they stick in the throat".
U.S. President Donald Trump acknowledged that his scheduled visit to Britain was coming at a time of "turmoil" - comments May later brushed aside - and two more junior ministers quit in protest, with reports that more were ready to go.More news: Turkey's Erdogan sworn in with new powers, names son-in-law finance minister
At 3pm on Monday, a statement was issued by Downing Street to say: "This afternoon, the Prime Minister accepted the resignation of Boris Johnson as Foreign Secretary".
Davis himself expressed regret that Johnson had quit, and said it would be "wrong" for his departure to trigger a major rebellion.
Lord Hague warned "Tory MPs with their pens hovering over letters" that the chances of such a challenge leading to the Brexit they desire "are about zero".
A Downing Street spokesman confirmed that if pushed to a confidence vote, May would not resign.
He was widely reported to have told the Chequers meeting on Friday that putting a positive gloss on Mrs May's Brexit package would be like "polishing a turd", though he later joined other ministers in signing up to the package.
Her proposal would see Britain adopt European Union rules for trade in goods after Brexit, but maintain flexibility for its key services sector and end freedom of movement.
"He said it here in Dublin previous year, that he didn't want a Norway type agreement because he felt that Britain would be rule takers - and that's the fundamental difficulty, Brexiteers are failing to grasp that when you enter an agreement with 27 other countries you agree to share a sovereignty".More news: #WorldCup - Croatia vs England preview
"Politicians come and go but the problems they have created for people remain", said Mr Tusk.
"I'm pleased David Davis has resigned, I'm pleased that Boris has chose to step aside and I think this Prime Minister needs to go". "But. who knows?", he added, wondering if Britain might reject the divorce.
"The general direction of policy will leave us in at best a weak negotiating position, and possibly an inescapable one", he said.
May's spokesman said it was positive for the United Kingdom that the former foreign secretary had a good relationship with the president.
Chequers is already unacceptable to many in her party and that's even before she gives away more concessions as part of her negotiations with Brussels: trying to steer this through Parliament on the back of Tory votes looks an impossible task.
Davis had reportedly threatened to resign several times over compromises that May sought with the European Union, only to back down at the last minute.More news: Ozil should quit Germany, says father