Commonwealth leaders said in a statement, according to Sky News: "We recognise the role of the queen in championing the Commonwealth and its peoples. The next head of the Commonwealth shall be His Royal Highness Prince Charles, the Prince of Wales."
While Prince Charles is the hereditary heir of 16 countries in the Commonwealth, he was not guaranteed to be chosen as the symbolic leader of the entire organisation.
The decision comes after the Queen publicly backed her son as the next Commonwealth leader for the first time.
"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," the 92-year-old said on Thursday during the formal opening of the Commonwealth Heads of Government Meeting at Buckingham Palace.
"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," she continued.
Moments before she spoke, Charles made an informal pitch for the role as he described the Commonwealth as a "fundamental feature" of his life.
"For my part, the Commonwealth has been a fundamental feature of my life for as long as I can remember, beginning with my first visit to Malta when I was just 5 years old," he said, in his own opening remarks at the summit.
"And so, Ladies and Gentlemen, I pray that this Commonwealth Heads of Government Meeting will not only revitalize the bonds between our countries, but will also give the Commonwealth a renewed relevance to all citizens, finding practical solutions to their problems and giving life to their aspirations."
"By doing so, the Commonwealth can be a cornerstone for the lives of future generations, just as it has been for so many of us."
There had previously been calls for the role to be rotated around the 53 member-states, most of which are former British territories.
British Labour politician Jeremy Corbyn was vocal in his opinion that Prince Charles shouldn't automatically inherit the top job.
"I think the Commonwealth ought to really get a chance decide who its own head is.The Queen is obviously very personally committed to the Commonwealth," he said on BBC programme Andrew Marr Show.
"After her, I think it's time for the Commonwealth to decide who its own president is on a rotational basis."
While Commonwealth Secretary-General Baroness Scotland opted for a more diplomatic explanation when quizzed on the matter, saying the group "will make a decision in whatever way they determine."
Her Majesty has been the ruler of the Commonwealth since she took to the throne in 1952. She will continue to lead the group until her death or if she abdicates.