In a heartfelt tribute to the Duke of Edinburgh, Sir John said that he had been the person to whom the monarch could unburden herself when faced with “a sea of problems”.
The Duke’s death on Friday will leave “an enormous hole” in the life of the Queen, whose role as head of state places her in a “lonely position”, said the former PM.
And he told BBC1’s Andrew Marr Show: “She has earned the right to have a period of privacy in which to grieve with her family.”
Sir John, who was appointed special guardian to princes William and Harry after the death of their mother Diana, got to know the Duke personally as they indulged their shared passion for cricket over many hours watching matches together.
He said that Philip had offered “astonishing” support in every way to the Queen during their 73 years of married life.
“Consider the position the Queen is in,” Sir John told Marr. “She is the head of state. That is a very lonely position in many ways.
“There are a limited number of people to whom she can really open her heart, to whom she can really speak with total frankness, to whom she can say things that would be reported by other people and thought to be indelicate.
“Of the handful of people to whom she could speak frankly, her husband Prince Philip was – obviously – the first one. And I’m sure that happened.
“That is why I think the Queen said at a later stage that he was her ‘great stay and support’. At times of difficulty, he was the person who was there. He was the person to whom she could unburden herself.”
Sir John added: “When you’re facing a sea of problems, as she so often was, and sometimes when you are overwhelmed by what has to be done, someone who understands that, someone who can take part of the burden, someone who can share the decision-making, someone who can metaphorically – or in the case of Prince Philip, I think, probably literally – put their arms around you and say ‘It’s not as bad as you think, this is what we have to do, this is how we can do it, this is what I think’.
“I think when you talk of him being the great support, that was it.”
Sir John said it will be “difficult” for the Queen to manage without her husband of more than seven decades, but that as “a stoic and a remarkable public servant” he had no doubt she will continue with her work.
“There are no doubt millions of people watching this programme who’ve lost a partner, a spouse, and it is a very lonely time,” he said.
“The Queen and Prince Philip had 73 years of marriage together. That is extraordinary. I can think of no-one else who’s had a marriage of that length in my experience.
“So it will be an enormous hole in her life that suddenly Prince Philip isn’t there.
“How will the Queen manage? Well I think there’s several things to say about that.
“Firstly, I hope she will be given some time and space. I know she is the monarch, I know she has responsibilities, but she has earned the right to have a period of privacy in which to grieve with her family.”
Looking to the Queen’s future, Sir John said: “Prince Philip may physically have gone but he will be in the Queen’s mind as clearly as if she was sitting opposite him. She will hear his voice, metaphorically, in her ear, she will know what he would say in certain circumstances.
“He will still be there in her memory. The echo will be there, and it always will be. It is with very close relationships.
“And I think after that, the Queen is both a stoic and a remarkable public servant. She will return to her work.
“But I do hope she’s given a little space and a little time and a little freedom to grieve in the way anybody else would wish to do after having lost their spouse.”