Experts say that as her children and grandchildren step up their royal duties, the transition to the next generation is an unstable time that could raise doubts about the monarchy's value in today's world.
"This is the end of an era and could bring into question the leadership of monarchy and wider questions of the role of the monarchy in 21st century Britain," said David McClure, the author of "The Queen's True Worth: Unravelling the Public & Private Finances of Queen Elizabeth II."
"Prince Philip's death will have a knock-on effect on people reconsidering the worth of the monarchy to Britain's life and as a political institution," he said.
In the U.K., the queen has a formal role as head of state, head of the Church of England and head of the armed forces and as a powerful symbol, giving a speech setting out the government's priorities at the start of the parliamentary year and formally signing off on legislation.
Britain isn't the only place where she is head of state. She is also queen of Australia, Canada, New Zealand and several island nations, as well as head of the Commonwealth, an association of 54 countries, almost all of which were once under British rule.
It is in those places where the transition to the next generation will start to raise the most questions, the historian Sarah Gristwood said.
"The British monarchy is always going to be most vulnerable in the years ahead not in Britain, but in the Commonwealth or other states that at present have the queen as head of state but that may not wish to do so forever," said Gristwood, author of "Elizabeth: The Queen and the Crown."
The day after Philip died Friday at age 99, the couple's firstborn, Prince Charles, referred to the Commonwealth twice in his short speech remembering his father. That was no accident, Gristwood said.
Support for the monarchy as an institution remains high in the U.K. More than 60 percent of those polled think Britain should have a monarchy in the future, according to a survey by YouGov in December. Only 25 percent said it should have an elected head of state.
In Australia, however, longtime critics of the monarchy are looking at the transition to the next monarch as a time to cut ties.
"After the end of the queen's reign, that is the time for us to say, 'OK, we've passed that watershed,'" former Prime Minister Malcolm Turnbull, who has campaigned to remove the British monarch as the country's head of state, told the Australian Broadcasting Corp. in March. "Do we really want to have whoever happens to be the head of state, the king or queen of the U.K., automatically our head of state?"
Meanwhile, in the Caribbean island nation of Barbados, where the queen is also head of state, the governor-general said in September on behalf of the government that "the time has come to fully leave our colonial past behind" and that "Barbadians want a Barbadian head of state."
In the U.K., despite the royals' high poll ratings, detractors are convinced that succession will bring increased resistance to the institution.
"When people think about the monarchy, they think about the queen or Philip and the link back to the past, the war and so on," said Graham Smith, chief executive of Republic, an anti-monarchy campaign group. "Charles will inherit the throne, but he won't inherit the deference or respect his mother has."
That hasn't escaped the attention of the royals. They are, indeed, aware of the perils of the transition and are already planning for it, the royal expert Daisy McAndrew said.
"One of the first things that is planned" when Charles takes over "is a 100-day tour of Great Britain, going all over the country. They will be trying to create a buzz around the accepted new monarch," she said. "That will be a make-or-break moment for Prince Charles to get the country behind him."
As the queen has aged, Charles has already taken on many of her duties, including overseas trips. His wife, Camilla, the Duchess of Cornwall, as well as Prince William and his wife, Kate, the Duchess of Cambridge, have also taken on extra responsibilities.
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But polls show that Charles' popularity is nowhere near that of the queen. According to a December YouGov poll on who should take over for the queen, 32 percent of respondents named Charles; 40 percent said William.
On a practical level, that may not matter. No U.K. political party supports getting rid of the monarchy, said Antony Taylor, a modern British historian at Sheffield Hallam University.
"Without a political party committed to reforming or removing the head of state, I don't see how you can institute change," said Taylor, who studies republicanism.
That, however, may change, as younger generations with no memory of the royal family's role keeping up the spirits of the nation during World War II grow up.
"For them, things are very fluid, and maybe a fluid situation gives the opportunity for them to think the unthinkable," he said.