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He is expected to stay on as a “caretaker” leader until the autumn, but some have questioned whether he can hold the position after more than 50 members of his Government resigned this week.
The race to replace Mr Johnson is shaping up to be one of the most open in recent memory, with no obvious successor to take over.
Prime Minister Boris Johnson - In pictures
Following his announcement, it will be up to the Tory 1922 backbench committee and the party HQ to announce plans for the leadership contest.
But MPs will be desperate to start the process as soon as possible so that a new leader can be in place by the time the Conservative Party holds its annual conference in Birmingham in October.
Before the PM had even quit, Attorney General Suella Braverman confirmed she would run to replace him.
“I am putting myself forward because I believe that the 2019 manifesto presents a bold and inspiring vision for our country,” Ms Braverman told BBC Radio 4’s Today programme this morning. “I want to deliver on the promises contained in that manifesto.”
Brexiteer Steve Baker also indicated he would stand in any future leadership election contest. “Some people I deeply respect are telling me, even imploring me to do it. And so I must consider it seriously,” he said.
“The Conservative Home poll keeps putting me in the top 10…it would be wrong of me to take it lightly. But I am realistic that it’s seems to me quite improbable that the rebel commander… with no Cabinet experience should win.
“But equally, it would be wrong of me to lightly dismiss serious people saying I should be Prime Minister.”
However, the bookmakers’ favourites to take over running the country are senior Tory MPs who have held top Cabinet positions.
International trade minister Penny Mordaunt was among those at the top of the list this morning.
The Portsmouth North MP became the first ever female Defence Secretary in 2019 but was demoted under Mr Johnson’s leadership.
It was speculated that she fell out of favour for backing the Prime Minister’s rival Jeremy Hunt in the last leadership race.
Former chancellor Rishi Sunak, who dramatically quit on Tuesday night sparking the onslaught of resignations, is also among the favourites to take over. In his letter to the PM, he said he had “reluctantly come to the decision that we cannot continue like this”.
But he has faced a number of his own scandals while in No 11. In April he issued an “unreserved apology” after being fined £50 for breaching Covid regulations for attending the Prime Minister’s birthday party on June 19, 2020.
He also faced criticism after reports his billionaire wife Akshata Murthy was non-domiciled in the UK for tax purposes. Mrs Murthy’s status meant she was not liable to pay UK tax on overseas earnings, as well as a host of other streams of income.
Defence Secretary Ben Wallace has impressed Tory members with his leadership over the war in Ukraine. The former British army captain refused to resign from Government as seven of his Cabinet colleagues quit.
He said today: “A number of us have an obligation to keep this country safe, no matter who is PM. The party has a mechanism to change leaders and that is the mechanism which I advise colleagues to use. In the meantime, the public would not forgive us if we left these Offices of State empty.”
Liz Truss is also at the top of the potential candidates. The Foreign Secretary has been in post since last September’s reshuffle and stood by Mr Johnson as his Government went into freefall.
The leadership election will take place in two stages with Conservative MPs requiring a proposer, seconder and some supporters before putting their own names forward to lead the party.
MPs then vote in a series of rounds to whittle down the candidates with contenders eliminated if they are unable to meet a certain threshold of support in the first two ballots.
Subsequently, the candidate who comes last is eliminated until there are only two remaining. Those two candidates are then put to the full national Tory Party membership to choose their preferred leader.
Although the first part of the process can be relatively quick, the second phase can take weeks as the final two present their pitches to the Tory grassroots.
In the last contest, won by Mr Johnson in July 2019, he won with 66 per cent of the party membership vote. His rival, Jeremy Hunt, secured just 34 per cent.
Other candidates who stood for leader in 2019 included Michael Gove, Sajid Javid, Rory Stewart, Esther McVey and Andrea Leadsom. Three contenders — James Cleverly, Sam Gyimah and Kit Malthouse —dropped out before the race formally began.
Mr Javid, whose Tuesday evening resignation as health secretary set the ball rolling on the crisis which has forced Mr Johnson out, is expected to mount another bid for the party leadership this week.
His damning statement on Mr Johnson’s leadership in the Commons yesterday was seen by some at Westminster as part of a possible campaign for the top job.
“I do fear the reset button can only work so many times,” he told MPs. “There’s only so many times you can turn that machine on and off before you realise something is fundamentally wrong.”
Nadhim Zahawi, who was made Chancellor by Mr Johnson on Tuesday night, is also expected to run for the leadership.
Believed to be one of the richest politicians in the House of Commons, he helped found polling company YouGov, and his business background could be seen as an asset as a time when the UK economy is facing stuttering growth and soaring inflation.
He has already said nothing is off the table when asked if he was considering tax cuts.
Jeremy Hunt, who urged fellow Tory MPs to vote against Mr Johnson in last month’s confidence vote, is also likely to run again.
Hannah White, from the Institute for Government, said that considering the high number of candidates likely to be interested in standing this time round, the 1922 Committee may look to raise the thresholds MPs need to hit to enter and remain in the contest.
“The indications are that there will be a wide variety of people considering running and given that there’s likely to be an imperative on the Conservative Party to get on with it, they might consider changing the thresholds,” Ms White said.