"This is the moment to chuck Chequers", Johnson said to applause and shouts of "bravo" at the Conservative Party conference in the English city of Birmingham on Tuesday. But he has also drawn criticism for his leadership aspirations.
Mixing breezy jokes with biting one-liners that always stopped short of attacking May herself, the former foreign minister called her strategy "dangerous and unstable".
But Johnson's recent comments about her Brexit plan, calling it "deranged" and saying it strapped a suicide vest to the British constitution, have angered many fellow MPs.
Scottish Secretary David Mundell said people were "concerned about Mr Johnson's behaviour".
She moved within months to start the Brexit process and sought to bolster her domestic political position with a snap election in June past year.
When asked once what was the naughtiest thing she had ever done, May admitted to running through fields of wheat as a child.
Under her plans, people and businesses who do not pay tax in Britain will face a surcharge of between 1% and 3% when they buy a property, with the money funding measures to tackle rough sleeping, the newspaper said.
But the conference has been dominated by Brexit, with eurosceptic lawmakers attracting hundreds of Conservative members to their events on the fringes.
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Ian Livermore, 65, from south Gloucestershire said the speech was "superb" and showed why Johnson should be leader.
He said: "Building a bridge between mainland Britain and Ireland, the latest intervention of Boris Johnson, who normally burns bridges instead of building them". But undoubtedly the biggest reaction came from his attack on the Prime Minister's Brexit proposals; cheers and enthusiastic clapping as he urged the party to "chuck Chequers".
In remarks that fuelled speculation about his leadership ambitions, the man who spearheaded the Leave campaign contrasted his position on Brexit with that of Mrs May, who backed Remain, saying: "Unlike the Prime Minister, I fought for this". "My letter of no confidence (in the prime minister) is in there as a marker on the ground".
Asked on BBC1's Breakfast what her relationship with Mr Johnson was like, she laughed and said: "Well, I'm sure that's going to be a very lively event this evening".
"We believe that we have produced a proposal which can operate within the current framework of technology and administration to deliver a free flowing border with no infrastructure on the island of Ireland within the boundaries of a free trade agreement", Baker told BBC radio.
Mary Wylie, a local party official from Devon in southwest England, said Johnson's speech expressed "my Conservative philosophy".
He urged delegates to persuade the PM to "chuck" Chequers and return to the policies set out in her Lancaster House speech of January 2017, something he said would be a "win-win" for both Britain and the EU.
And she will look to turn the tide of internal party anger towards Jeremy Corbyn's Labour, suggesting on the back of the anti-Semitism row that it is now the new nasty party with the Conservatives as the party of patriotism, business, aspiration and "above all a party of Unionism".
"But we have been very clear, we have got to deliver a deal for the United Kingdom that's good for our economy, make sure people continue to have the opportunity to have job security and job opportunities for the future and respect that referendum and deliver on getting back control of our border, of our laws, of our money and that's what this package does".