In an unexpected move, the Queen told Commonwealth leaders gathered at Buckingham Palace for the formal opening of this year’s summit that she wanted the Duke of Rothesay to continue her work at the head of the organisation that brings together Britain and many of its former colonies.
Commonwealth leaders will decide who will succeed the Queen as head of the organisation at a retreat on Friday at Windsor Castle, where discussions are set to be held in private without aides or advisers present.
There have been calls from some quarters for the role to be taken away from the Royal Family and handed to member governments on a rotating basis, including this week from Labour leader Jeremy Corbyn.
Prince Charles is said to have widespread backing to continue the Queen’s role, including from Theresa May.
At the formal opening of the summit, with Charles and other senior royals sat in front of her, the Queen told delegates: "It remains a great pleasure and honour to serve you as Head of the Commonwealth and to observe, with pride and satisfaction, that this is a flourishing network.
"It is my sincere wish that the Commonwealth will continue to offer stability and continuity for future generations, and will decide that one day The Prince of Wales should carry on the important work started by my father in 1949.
"By continuing to treasure and reinvigorate our associations and activities, I believe we will secure a safer, more prosperous and sustainable world for those who follow us: a world where the Commonwealth's generosity of spirit can bring its gentle touch of healing and hope to all."
The prime minister of Malta, Joseph Muscat,who is the outgoing chair-in-office of the Commonwealth, also backed Prince Charles as head of the Commonwealth, seeming to confirm the prince's future role.
"We are equally elated by the vigour with which His Royal Highness the Prince of Wales actively participates in Commonwealth affairs and puts a strong Commonwealth dimension in his various national and global ventures," Dr Muscat said.
"We are certain that, when he will be called upon to do so, he will provide solid and passionate leadership for our Commonwealth."