Speculation about whether the heir to the throne would succeed his mother, who has been head of the Commonwealth since coming to the throne in 1952, has heightened in recent weeks.
In an small moment of history the Queen has, for the first time, publicly referred to the day when she will no longer reign over us.
The Prince of Wales, who is long understood to have coveted the title, told leaders "the Commonwealth has been a fundamental feature of my life for as long as I can remember".
He hoped the 2018 summit would give the group "renewed relevance" to citizens, making it a "cornerstone" for future generations, as it had been for him.
The prime minister also thanked the Queen for hosting the event, calling the monarch a "steadfast and fervent champion" of the Commonwealth.
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This week Malcolm Turnbull again restated the Government's view that the "monarch of the United Kingdom" should hold the role.
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The leadership discussions come amid a wider debate, however, about whether the Commonwealth should transform into a global leader on health, education and the environment, or whether the ageing and bureaucratic institution has already outlived its usefulness.
"Most countries in the Commonwealth are in fact republics", he said.
Addressing the gathering of dignitaries, royals and the prime minister, the Queen said it was a "pleasure, this time, to welcome you to my home" for the biennial meeting.
"Spanning so many decades, so many leaders, so many chapters of history".
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You are not alone! "Please share my story!" In fact, we are saving a seat for you at our lunch table in the clubhouse. Her father added that they might reconsider if the bullying continued.
"Succession is a matter for the Commonwealth as a whole to determine". "We are certain that, when he will be called upon to do so, he will provide solid and passionate leadership for our Commonwealth".
The meeting, which held on Thursday at the Lancaster House in London, was declared open by Queen Elizabeth II.
Prime Minister Theresa May told the leaders the summit would "take on some of the 21st Century's biggest questions". "I consider myself fortunate over the years to have been able to meet and talk with so numerous giants of the Commonwealth".
Coldstream Guards carry flags of 53 Commonwealth countries.
The British hosts have set out four main goals for the summit.
Trudeau is expected to raise his voice against the use of plastics and pitch in LGBTQ rights on Thursday, media report said. The UK is considering banning cotton buds, plastic drinking straws and single-use plastics in England starting in 2018, part of a larger campaign to halt pollution of the world's rivers and oceans.
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She has spoken on a number of occasions about her enthusiasm for charity work particularly causes linked to female empowerment. The event involves charities and organizations that work to promote global gender equality through girls' education.
Given its highly diverse membership, if agreements can be reached within the Commonwealth, they can likely achieve wider support.