Mrs May confirmed on Friday that she will resign as party leader on 7 June, but will continue as PM while the leadership contest takes place.
After weathering a litany of political setbacks, why does Mrs May's resignation come now?
But his supporters say Johnson, a favorite of party activists, has the star quality the party needs to win elections and curb the populist threat from Nigel Farage, an adept political campaigner.
May shared her speech with millions as camera crews from around the world captured her dramatic resignation announcement in front of the iconic door to 10 Downing Street.
Reports circulated throughout the week that the Prime Minister would resign Friday, after repeated failures to secure a Brexit deal that would pass through the British Parliament while simultaneously appeasing exasperated European Union negotiators in Brussels. Nominations are likely to start on June 10 and once closed Tory parliamentarians will vote in a series of rounds to whittle down the candidates to a final two.
It means May still has the task of hosting US President Donald Trump during his state visit early next month. Other ministers also threatened to resign if May refused to set a timetable for her departure.
She agreed with chairman of the Tory backbench 1922 Committee, Sir Graham Brady, that the process to choose a new leader should begin the week after she stands down.
"There are huge tensions in this race which are that people will be encouraged to promise things they can't deliver, of those probably the most dramatic are people who are going to be encouraged to promise a no-deal Brexit", one of the contenders, Rory Stewart, told BBC radio.
But while May's departure now makes "no deal" more likely, there is stiff opposition to this in parliament and many MPs could try to stop it by demanding a second referendum on Brexit.
Following the resignation of Prime Minister Theresa May on Friday, almost two-thirds of Britons believe the U.K.is in a state of crisis, with most favoring a general election once a new leader is in place, according to a new survey. Leadsom, who came second in a leadership bid in 2016, was heavily criticized at the time for saying that being a mother would give her an advantage as prime minister.
Mr Rory Stewart said he would not serve under rival Boris Johnson because of his backing for a no-deal exit. The surprise is not that the prime minister has gone but that it took so long for it to happen.
For now, nothing is certain except that May's successor will have to pick up the pieces in the hopes of resolving an issue that has been dividing the country.
In a tearful speech on the steps of 10 Downing Street, May said she had done her best to honor the result of the 2016 European Union referendum.
"To succeed, he or she will have to find consensus in Parliament where I have not", she said.
The Daily Telegraph leads with leadership hopeful Boris Johnson's vow to take Britain out of the European Union on October 31 "deal or no deal" if he succeeds Mrs May as PM.
May bequeaths a deeply divided country and a political elite that is deadlocked over how, when or whether to leave the EU.
May will stay on as a caretaker prime minister until the new leader is chosen, a process the Conservatives aim to complete by late July.
A sticking point for many Conservatives is the "backstop" inserted in May's deal to avoid a threat to the peace process in Northern Ireland, which would keep the United Kingdom in a form of customs union with the EU. Parliament has voted to rule out a no-deal Brexit, though it remains the legal default option. There has been talk of an alliance between Johnson and the former Remainer, Amber Rudd.
But Brussels is already warning that it won't tolerate a bid by May's successor, whoever it is, to seek any changes or serious tweaks to the Brexit Withdrawal Agreement concluded with May after two years of haggling.