Queen Elizabeth II was head of the Commonwealth for as long as she reigned.
The title isn't inherited, but Commonwealth members have already agreed that King Charles should succeed the Queen.
Her death doesn't change a lot about how the Commonwealth runs, but it could prompt the question of whether it has a purpose, experts say.
It's a "watershed moment", which may spark a rethink of the Commonwealth's role, according to constitutional law expert Anne Twomey.
Philip Murphy, former head of the Institute of Commonwealth Studies, said the organisation lent on the monarch for legitimacy, but had achieved "nothing tangible" on its own.
What is the Commonwealth?
It's a voluntary association, sometimes described as a "family of nations".
The Commonwealth is made up of 56 countries, but only 15 are realms – countries where the monarch is head of state (and this includes the United Kingdom).
Five of those are in the Asia Pacific: Australia, New Zealand, Papua New Guinea, Tuvalu and Solomon Islands.
A country can become a republic (and lose the monarch as sovereign) and stay in the Commonwealth, as Barbados did earlier this year, and which others countries are considering.
Also, not all Commonwealth members were British colonies, although most were once under British rule.
The 'decoloniser' Queen
Earlier this year Prince William and the Duchess of Cambridge were met with protests and demands for reparation in Jamaica.
Jamaica has also declared its move to become a republic – on the same visit, Prime Minister Andrew Holness told the royal couple his country was "moving on".
The Queen often said that the modern Commonwealth was a break from colonialism – a voluntary, equal organisation that "bore no resemblance to the empires of the past", as she said in 1977.
Sue Onslow, deputy director of the Institute of Commonwealth Studies, said the Queen "oversaw Britain's transition from a global empire into being a medium-sized north European country", which had begun to face its past.
But the colonial link was not so easily dissolved.
The trend away from having the monarch at the helm would be the most significant change for the Commonwealth ahead – but it's one that was already well underway, Professor Murphy said.
"The change that everybody thought would be decently delayed until the Queen is dead, is [already] taking place," he said.
But he doesn't see much appetite for countries to leave the Commonwealth.
Professor Twomey said more countries would likely become republics – but she did not expect a huge push.
"That feeling of some kind of personal relationship with the Queen is going to be fractured, so countries will lose that attachment, but on the other hand there will be an enormous amount of nostalgia … and it’ll be interesting to see whether that wave of nostalgia conflicts at all with the movement we are seeing in the Caribbean, which is the growth of resentment at the consequences of colonisation," she said.
Is the Commonwealth at risk?
The Commonwealth had challenges before the Queen died.
One was that not many people really knew, or cared, what it did.
"From the Australian point of view most people don’t pay any attention to the Commonwealth, it’s really just a forum for us to win a lot of medals," Professor Twomey said.
There were far more small countries in the Commonwealth than large, donor members, so it was these developing nations that its future could hang on, Professor Twomey said.
"If the countries concerned, who are the recipients of the aid and support, actually don’t see the value in it anymore and are getting that kind of support through other means, then I think there is a real risk of the Commonwealth falling over," she said.
The Commonwealth had sentimental appeal in the Pacific – but little else, said Steven Ratuva, director of the Macmillan Brown Centre for Pacific Studies at the University of Canterbury.
"The Queen has been able to hold it together because of her deep sentimental connections with people," he said.
"Charles may not have the same depth of sentimental link, so there will be a struggle to keep the Commonwealth together because there are no strong economic, political or strategic alliances which hold it together.
"Much of the links are historical and sentimental and sentiments as you know can fluctuate and easily wither away.
"All you need is a trigger and then there might be one or two leaving, an exodus perhaps, and then the Commonwealth with its sense of illusions of grandeur of the past, might just disappear.
"And for some countries it may be no loss whatsoever."
'Dainty but formidable shoes to fill'
The Queen was the "invisible glue" that held the Commonwealth together, but her son was well prepared for the post, Dr Onslow said.
"He has the capacity for the role but I cannot pretend that he is beloved mother … we won’t see her like again," she adds.
"The prince has earned his spurs [but] those are dainty but formidable shoes."
Dr Ratuva says King Charles could be seen as a more progressive head.
"He is seen as a new generation, with new ideas at a time when people's thinking and expectations are changing, certainly in the Pacific," he said.
"He won't be seen as the matriarchal leader. I'm not too sure he will be seen as the loving patriarch, but certainly we will see something different in the way he will be perceived by the Commonwealth."
