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Mr Cameron’s wife Samantha, close friend and Conservative Party chairman Lord Feldman, chief of staff Ed Llewellyn and deputy Kate Fall were among the aides who gathered to watch TV coverage in the evening.
The Newcastle figures gave the PM the first indication that things were not going his way. And when Leave secured a big win in Sunderland the mood in the famous building darkened quickly.
At around 3am, with the outcome becoming clear, Mr Cameron held a council of war in his study with Chancellor George Osborne, Mr Llewellyn, Ms Fall, Lord Feldman and communications director Craig Oliver.
They discussed whether he should stay on, but he was adamant that his life would become impossible as Brexit MPs would be constantly at his throat.
Quoting Enoch Powell, he said: ‘All political lives end in failure.’
Half an hour later, Mr Cameron beckoned Cabinet Office minister Matthew Hancock into his study.
He was ‘calm, philosophical, and neither angry nor visibly upset’, according to extracts from Mr Seldon’s updated biography published in The Times.
Mr Cameron told the minister: ‘I’m going to have to go … I don’t want to lead a government where I don’t agree with its policy.’
Later the PM’s head of operations Liz Sugg asked if it was really necessary for him to stand down as he was ‘best person to lead this country’.
But Mr Cameron apparently replied that he had ‘made up my mind’.
As the moment when he would have to go outside and face the media approached, he and Samantha walked through the long corridor at Number 10 and were applauded by staff and officials.
Both the Camerons were overcome with emotion, and the premier told them: ‘You are the best team I could possibly have hoped for.’
Emerging from Downing Street grim-faced and hand-in-hand with his wife shortly afterwards, Mr Cameron stepped up to a government podium and said: ‘I will do everything I can as Prime Minister to steady the ship over the coming weeks and months but I do not think it would be right for me to try to be the captain that steers our country to its next destination.
‘This is not a decision I have taken lightly but I do believe it is in the national interest to have a period of stability and then the new leadership required.
‘There is no need for a precise timetable today but in my view we should aim to have a new Prime Minister in place by the start of the Conservative Party conference in October.’
He added: ‘Delivering stability will be important. And I will continue in post as Prime Minister with my cabinet for the next three months.’
Mr Cameron said he had spoken to the Queen this morning to alert her to his decision. He also said he would not be triggering Article 50 of the Lisbon Treaty but would instead leave it to his successor.
‘The negotiation with the EU will need to begin under a new Prime Minister and I think it is right this new Prime Minister takes the decision about when to trigger Article 50 and start the formal and legal process of leaving the EU,’ Mr Cameron said.
The British people have made a choice that not only needs to be respected but those on the losing side of the argument, myself included, should help to make it work.
‘Britain is a special country, we have so many great advantages – a Parliamentary democracy where we resolve great issues about our future through peaceful debate.
‘A great trading nation with our science and arts, our engineering and creativity, respected the world over.’And while we are not perfect, I do believe we can be a model of a multi racial, multi faith democracy where people can come and make a contribution and rise to the very highest their talent allows.’
He went on: ‘Although leaving Europe was not the path I recommended, I am the first to praise our incredible strengths. I have said before Britain can survive outside the EU and indeed that we could find a way.
‘Now the decision has been made to leave, we need to find the best way. I will do everything I can to help.
‘I love this country, and I feel honoured to have served it and I will do everything I can in future to help this great country succeed.’