He is divisive, and his stock has fallen lately. But the Whitehall mandarins and the British political class have long assumed he covets the keys to 10 Downing Street. His departure hints at a possible leadership challenge within May's Conservative party.
In his resignation letter, Johnson wrote that the Brexit dream "is dying, suffocated by needless self-doubt." He said that Britain was "headed for the status of colony - and many will struggle to see the economic or political advantage of that particular arrangement."
"I am sorry - and a little surprised," May wrote in reply.
Johnson's allies say he did the honorable thing by resigning. His critics see selfish manoeuvering.
May replaced Johnson today with Jeremy Hunt, formerly the Health Secretary, who successfully secured a big bump in spending for the underfunded National Health Service.
She named as Davis's successor as 44-year-old Dominic Raab, a leading pro-Brexit campaigner who served as her housing minister.
Culture Secretary Matt Hancock takes over at health, and Jeremy Wright, the Attorney General, takes over culture. His replacement is Geoffrey Cox.
But the bombshell resignations expose May to further confrontations with restive Conservative Party members outraged over what they see as the prime minister's plan for a "soft Brexit" that keeps Britain tied to many EU rules and regulations after it leaves the bloc in March 2019.
Backers of a hard Brexit, who want a decisive break from Brussels, are now in open revolt. They denounced May's latest road map as a fudge, a timid capitulation: "Brexit in name only" that ignores the 52 per cent of voters who opted in June 2016 to leave EU.
Tim Bale, a political expert at Queen Mary, University of London said that while May was in a difficult spot, "I don't think it's necessarily fatal for her - at the moment anyways."
He said the Conservative Party doesn't really have the appetite for another general election - because of the ongoing Brexit negotiations and because Tories haven't coalesced around a candidate to champion.
Johnson has "still got a bit of a fan club, but I'm not sure he's the pin-up that he once was," Bale said. While some see an English original, others see a clown.
May paid tribute to Davis and Johnson in Parliament today, even though "we do not agree about the best way of delivering our shared commitment to honour the result of the referendum."
When she praised Johnson for his "passion," jeering erupted in the chamber. When she said Brexit had generated "a spirited national debate" there were guffaws.
May said she had listened to every possible idea and concluded hers was right one to pursue.
She urged Brussels to seek compromise. "If the EU continues on this course, there is a serious risk it could lead to no deal, and this would most likely be a disorderly no deal," she said. "A responsible government must prepare for a range of potential outcomes."
Where May's Brexit plans go now is an open question. Business leaders in Britain who run companies that make airplanes and automobiles are clamouring for answers and warning that Brexit is drifting towards the rocks.
The pound sterling slid after the Johnson resignation, while the markets ticked up.
Across the English Channel, reaction was muted.
"Politicians come and go, but the problems they have created for their people remain," European Council President Donald Tusk said of Davis's exit, just before being informed of Johnson's resignation. He said the same sentiment extended to Johnson as well.
Tusk added: "The mess caused by Brexit is the biggest problem in the history of EU-UK relations, and it is still far from being resolved."
Trump is scheduled to arrive on Friday morning NZT for a visit that will be closely watched for any comments on Brexit and US relations with the European Union.
Last month, Johnson told an audience at a private gala dinner that he thought Trump would do a much better job at negotiating Brexit than his Prime Minister.
"Imagine Trump doing Brexit," Johnson told his audience of Tory activists. "He'd go in bloody hard … There'd be all sorts of breakdowns, all sorts of chaos. Everyone would think he'd gone mad. But actually you might get somewhere. It's a very, very good thought."
In Parliament, the hardline Brexit supporters are the most vocal but not the majority. A compromise exit is supported by moderate Tories, the Labour Party and the Liberal Democrats, among others.
In his letter of resignation, Davis warned May her approach will lead to further demands from Brussels and give Europe control of large swaths of the British economy.
One of the leading campaigners for leaving the European Union, the radio show personality and European parliamentarian Nigel Farage, said: "For Brexit to succeed we must get rid of this awful, duplicitous PM."
Davis suggested that May's promise that Britain and its parliament would "take back control" from Brussels was hollow. "This is painted as returning power back to the House of Commons," Davis said. "In practice, it is not doing so."
For two years, chief negotiator Davis has been the white-haired, ruddy-cheeked face of Brexit. But talks in Brussels were notoriously slow, because May's government could not - and still cannot - agree on what kind of future relationship Britain wants with Europe on trade, immigration, law, tariffs and border checks and security.
Recently it was revealed that Davis had only attended four hours of talks in Brussels in 2018, going as long as three months without meeting the EU's chief negotiator Michel Barnier.
David Lammy, a prominent member of the opposition Labour party, derided Davis as "a man who can't take responsibility. For two years he's been in charge of Brexit. No one in the world is as much to blame for this monumental mess as himself."
The prime minister's plan for a soft Brexit was pushed forward by May at a crunch Cabinet meeting at her countryside manor, called Chequers, at the weekend.
In that meeting, May had appeared to win over her fractious cabinet and secure approval for her plan, which was to be published as soon as this week in a lengthy White Paper that would stake out Britain's vision for future relations with Europe.
The brief outline that was released shows she supports a middle way of compromise with Brussels, keeping Britain closely aligned with Europe on standards, "a common rule book for industrial goods and agricultural products."
Jeremy Corbyn, the leader of the Opposition Labour Party, mocked May in Parliament today, saying it had taken her two long years to come up with a Brexit plan and only two days for that plan to unravel.
