The Prince of Wales gave his blessing on Friday to Commonwealth countries that want to sever ties with the royal family, insisting that such change can be made "calmly and without rancour".
Prince Charles, 73, told prime ministers and presidents gathered for the Commonwealth Heads of Government Meeting (Chogm) in Kigali, Rwanda, that whether members wanted the Queen as head of state or became a republic was a matter for them alone.
His comments come at a pivotal time as several countries, including Jamaica and Australia, are poised to follow Barbados in removing the Queen as head of state.
There are fears many others will become republics when the Prince becomes King, having maintained ties with the royal family only out of respect and loyalty to the Queen.
While there has been no suggestion members would go on to leave the Commonwealth, there is said to be concern at the palace that such moves will "loosen the ties that bind" and could lead to the long-term collapse of the union.
It came as the Prince also expressed his deep personal sorrow over the "painful history" of slavery, acknowledging that lessons must be learnt in order for the Commonwealth to move forward.
He told Commonwealth leaders the roots of the 54-member association "run deep into the most painful period of our history".
The Prince stopped short of an apology but said he was still learning, and continuing to deepen his own understanding "of slavery's enduring impact".
His speech at the Chogm opening ceremony came as new countries with no historic ties to the UK look to join the Commonwealth.
Prince Charles said: "Our Commonwealth family is – and will always remain – a free association of independent self-governing nations.
"We meet and talk as equals, sharing our knowledge and experience for the betterment of all citizens of the Commonwealth – and, indeed, the wider world."
He added: "The Commonwealth contains within it, countries that have had constitutional relationships with my family, some that continue to do so, and increasingly those that have had none.
"I want to say clearly, as I have said before, that each member's constitutional arrangement, as republic or monarchy, is purely a matter for each member country to decide.
"The benefit of long life brings me the experience that arrangements such as these can change, calmly and without rancour."
The Prince told delegates at the Kigali Convention Centre that the organisation was "uniquely positioned" to achieve positive change in the world, particularly on climate change and opportunities for young people.
"To achieve this potential for good, however, and to unlock the power of our common future, we must also acknowledge the wrongs which have shaped our past," he added.
"Many of those wrongs belong to an earlier age with different – and, in some ways lesser – values. By working together, we are building a new and enduring friendship."
He said that on a recent royal tour to Canada, he and the Duchess of Cornwall were "deeply touched" to meet those engaged in an ongoing process of reconciliation – "indigenous and non-indigenous peoples reflecting honestly and openly on the darkest aspects of history".
He went on: "It seems to me that there are lessons in this for our Commonwealth family. For while we strive together for peace, prosperity and democracy I want to acknowledge that the roots of our contemporary association run deep into the most painful period of our history.
"I cannot describe the depths of my personal sorrow at the suffering of so many, as I continue to deepen my own understanding of slavery's enduring impact."
A royal source said the Prince was keen to make a "personal" statement on the issue, having spoken of Britain's colonial history and the "appalling atrocity of slavery" last November, when Barbados formally became a republic.
The Prince said in a speech in Ghana in November 2018 that "the unimaginable suffering it caused, left an indelible stain on the history of our world".
In March, the Duke of Cambridge, echoed his father's words during a tour of the Caribbean, expressing his "profound sorrow" and adding that slavery was "abhorrent".
The Prince's speech to Commonwealth leaders was considered an opportunity to "set out his vision" for its future, having been elected the Queen's eventual successor as head of the Commonwealth in 2018.
He considers its power to be in its diversity, an aide said, and has been thinking deeply about what its priorities should be and "what it can do collectively, together".
As 60 per cent of its 2.6 billion population is under 30, he believes it "critical" to ensure young people have the opportunities, training and employment they need.
Members from Canada to the Seychelles are "massively impacted" by climate change and for the Prince to bring businesses to Chogm to discuss potential solutions was "critically important".
Both the Prince and the Queen have made clear they believe the Commonwealth can be a "force for good" if all nations work together.
In order to achieve that vision, the Prince understood that the "historic shared past" must be recognised, an aide said.
For him, that meant making a personal statement about his sorrow but also, his continued learning:
"It is recognition that he is listening and learning in order to determine future action."