The right of the Prince of Wales to become the next head of the Commonwealth is expected to be decided at a major meeting of the 53 countries that comprise the organisation in April.
Leaders from the countries will meet in London for the Commonwealth Heads of Government meeting (CHOGM), which is expected to be the final such meeting to be attended by the Queen.
The countries are likely to set out the plans for who will replace the Queen as head of the Commonwealth in a long communique issued at the end of the meeting, The Daily Telegraph understands.
Although the Prince of Wales will become King on the death of his mother, the head of the Commonwealth is not a hereditary position and there is no guarantee that the new King will follow the Queen into the role.
The Queen, who turns 92 in April, was proclaimed head of a much smaller Commonwealth at her coronation when she became head of state in seven of its eight members.
Prince Charles and Camillas tour of Asia gallery puff
Today the Commonwealth is much larger and the Queen is the head of state of 15 realms among its 53 members, mostly former constituents of the British Empire.
One source said: “As part of the conversations at CHOGM it is perfectly natural that there will be a conversation at some point about succession going forward.”
A second source said: “It [the succession] will be discussed at CHOGM, no question. Because Britain is hosting it this year they want to bring it to a head. What they don’t want is for the Commonwealth to split up, to become irrelevant.”
For years, it has been widely assumed that the Prince of Wales will become Head of Commonwealth.
He has previously represented the Queen at CHOGM, with two major tours to Commonwealth countries in the last year and a lifetime of relationship with its leaders.
During a visit to Singapore in the autumn, he delivered a significant speech hailing the “special importance” of the Commonwealth “family”, and is expected to take a prominent role in CHOGM meetings in April.
In a 2015 speech to CHOGM, the Queen signalled her deep support for her son, saying she could not “wish to have been better supported and represented in the Commonwealth than by The Prince of Wales who continues to give so much to it with great distinction”.
A new “high level group” looking at the governance of the Commonwealth Secretariat – which was set up at the last CHOGM meeting in Malta in 2015 – met for the first time in London on Tuesday.
Commonwealth figures are very sensitive to concerns from smaller members that the organisation is dominated by the so-called ABC white Commonwealth countries – Australia, Britain and Canada .
One source said: “They are trying to make sure that the smaller nations have just as much say if not more on certain issues. Deploying Harry is very important.”
Prince Harry is expected to take on more Commonwealth roles in a bid to modernise the Commonwealth and to “re-energise” the organisation and make it “more relevant”, according to a source.
The Prince is expected to take a leading role in the Queen’s Commonwealth Canopy project which was first proposed by Commonwealth countries in 2015 to help protect forests. The Prince visited one scheme in Epping last year.
The Royal Commonwealth Society has recently opened new a new office in Washington DC and a “Nordic-Baltic Hub” based in Helsinki to reach out to Finland, Denmark, Estonia, Iceland, Latvia, Lithuania, Norway and Sweden.
The hope is that the Commonwealth – and its role in connecting its member states - will become more relevant to the UK after Britain leaves the European Union next year.
At a glance | Current line of succession to the British throne
Tim Hitchens, a senior Foreign Office official and former ambassador to Japan, was put in charge of a team preparing for the Commonwealth summit in London last year before talks on the succession started.
Mr Hitchens, a former assistant private secretary to the Queen, is based in the Cabinet Office next to 10 Downing Street and will report directly to Theresa May, the Prime Minister.
The secretariat helps run the group of 53 mostly former British colonies that make up the Commonwealth and that are home to some 2.3 billion people, more than a quarter of the world's population.
A Buckingham Palace spokesman said any decisions about succession were a “matter for the Commonwealth”.