The British head of state, Queen Elizabeth II, turns 92 today, although her birthday is not officially celebrated until June.
However, the position is not hereditary, and some people have suggested a non-royal leader would give the group of nations a more modern profile.
Speaking after the Commonwealth Heads of Government (CHOGM) Meeting Theresa May expressed her gratitude to the Queen for her years of service and said of Prince Charles: "His Royal Highness has been a proud supporter of the Commonwealth for more than four decades... it is fitting he will one day take over the role of head of the Commonwealth from the Queen".
A specially invited audience seated in the Ballroom of Buckingham Palace was introduced to Heads of Government and senior leaders from 53 Commonwealth Member Countries, as well as the Commonwealth Secretary-General Patricia Scotland.
The decision comes after the Queen publicly backed her son as the next Commonwealth leader for the first time.
The Commonwealth is a community of 53 countries - mostly former British colonies - with a combined population of about 2.4 billion.
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During the opening of the Commonwealth Heads of Government Meeting, she told them it was her "sincere wish" that the family of nations would one day decide the prince should carry on the Commonwealth work started by her father King George VI. Today, though, that changed when the United Kingdom royal family matriarch gave her support to her oldest child, Prince Charles.
"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 Canada Justin Trudeau said he "very much agree" with the desire of the Queen.
The Commonwealth Heads of Government will meet in retreat for two days to discuss matters relating to the theme: "Towards a Common future".