The King is 'fully open' to being replaced as head of state in Caribbean countries – if that is the will of their people.
His Majesty remains 'ready to serve', but will not stand in the way if countries decide he is no longer wanted, senior aides have made clear.
It comes as debate continues to rage over the legacy of empire and the issue of reparations following the Prime Minister's controversial intervention on the eve of the Commonwealth Heads of Government Meeting in Antigua last week.
Andy Burnham's offer to hold talks over a formal apology for the historic transatlantic slave trade has sparked a wave of calls in the region for Britain to pay billions in compensation – and left the King walking a diplomatic tightrope.
It has also shone a spotlight on a wider conversation about the monarchy, with Antiguan prime minister Gaston Browne announcing he wants to see his country become a republic even while the King was his guest.
Speaking at the close of his high-profile tour, a senior royal aide said: 'The King and the Royal Family are there to serve the people of these regions for as long as they wish.
'But if they don't wish it any more, then we really are fully open to that.
'The family serves when it's wanted and if not, then a new arrangement can be found.'
King Charles and Queen Camilla pose for a official tour photo to mark the conclusion of the trip
Charles meets Prime Minister of Antigua and Barbuda, Gaston Browne on November 1
Charles speaks to Antigua and Barbuda's Governor-General Rodney Williams as he arrives at VC Bird International Airport on November 4
Charles remains head of state in 14 realms outside of the UK, seven of which are in the Caribbean: Antigua and Barbuda, the Bahamas, Jamaica, Grenada, Saint Kitts and Nevis, Saint Lucia and Saint Vincent and the Grenadines.
Under his mother, Queen Elizabeth II, 17 realms transitioned to become republics, although all remained in the Commonwealth.
Charles has visited the Caribbean dozens of times as heir. His recent three-country tour, taking in the Bahamas, Guyana and Antigua and Barbuda is his first as King.
Speaking candidly about the sovereign's role, aides say Barbados is an example of a country that made a successful transition from a realm to a republic in 2021.
'We agreed how we would do it. It would be done without rancour,' a source said.
'We've got absolutely no difficulty with that. It's really all a matter of what countries want to do.
'You'll have seen that the King was delighted to go along to the events which marked Barbados's transition into a republic.'
Diplomats consider the monarch's eight-day tour a huge success in terms of its main objectives, to shore up trade links and develop co-operation in key areas such as the environment.
However the trip was also dogged by the growing row over slavery and reparations, stoked by Mr Burnham, who rowed back on previous refusals by successive British governments to even entertain a formal public apology over the historic transatlantic slave trade.
That has sparked a dramatic escalation in demands for 'reparatory justice' for the region and put Charles, as head of the Commonwealth, in a particularly tricky position.
Charles and Prime Minister Andy Burnham engage in conversation during an official dinner at the Commonwealth Heads of Government Meeting on November 3
Charles and Camilla wave as they depart Antigua and Barbuda on November 4
King Charles, Queen Camilla and Commonwealth Secretary-General Shirley Botchwey attend a Commonwealth Heads of Government Dinner on Tuesday
Speaking to ITV News just hours after attending church with the King and Queen on Sunday, Gaston Browne said he had great respect for Charles personally, but repeated his view that Antigua should replace him as head of state.
'I am a republican. So if you asked me about my personal view, I would like to see Antigua and Barbuda become a republic... but I have to recognise and accept the fact that there are certain constitutional provisions to become a republic, and that, ultimately, it is the decision of the people,' he said.
The constitution requires more than two-thirds of Antiguans to vote to replace the British monarch and change the constitution.
He added: 'So until such time as the question is put to them, I have to accept that King Charles remains.'
Mr Browne also reiterated his demands for Britain to pay reparations.
'I understand the politics in the UK, in which it may be a difficult proposition for him to agree to any form of reparations, but that does not negate the need for reparations,' he said of Mr Burnham.
Sources close to the King have insisted he has a 'good relationship' with Mr Burnham, despite the furore.
He apparently makes a point of trying to find something to connect over with all his prime ministers, no bad thing given he has had four in five years.
The aide said: 'The King very quickly finds a way to establish a good working relationship with the sitting prime minister. I see them together every week, and it genuinely is a good relationship.'
They said of Mr Burnham's announcement: 'He's perfectly entitled to do that. He is the head of the elected government.
'If that's what elected politicians want to do, it's not for us to get in the way.'
Asked whether the King would himself ever consider an apology over his own family's links to the slave trade, the aide said coyly: 'The King is the Crown, the Crown is the state, the state is run by an elected government, so we have to see how this whole situation plays through.'
They did confirm, however, that the Royal Collection Trust, the organisation responsible for the priceless collection of arts, gems and antiques held by the monarch on behalf of the nation, does have a 'clear restitution policy' by which countries can apply for items to be returned if there are questions over how they were acquired.