The ceremony in the Sistine Chapel, broadcast live by the Vatican's official news service, came during a state visit by the 76-year-old monarch and his wife Queen Camilla.

It was the first time a reigning English or British monarch has prayed publicly with a pope since English king Henry VIII broke with Rome 500 years ago.

Triggered by the then pope's refusal to annul Henry's marriage so he could marry another woman, the schism made the monarch head of the separate Church of England.

Charles and Camilla earlier had their first meeting with Pope Leo, who took over as head of the world's 1.4 billion Catholics in May following the death of Pope Francis.

The US pontiff led the service beneath Michelangelo's spectacular ceiling frescoes with the archbishop of York, Stephen Cottrell, currently the senior cleric of the Church of England.

Charles and Camilla sat at the front of the chapel alongside the pope and the archbishop, facing an audience including Catholic and Anglican clerics, politicians and diplomats.

The service brought together Catholic and Anglican traditions, with the choir from the Sistine Chapel joined by that from Saint George's Chapel, Windsor Castle, one of the king's residences.

It was centered on conservation and protecting the environment, a cause long championed by Charles.

The 76-year-old monarch, officially supreme governor of the Church of England, flew to Rome on Wednesday evening for what Buckingham Palace described as a "historic" trip.

The royals were greeted at the Apostolic Palace on Thursday morning by a ceremonial guard of honor by the Swiss Guard, the pope's colorful private bodyguards, before a private meeting with Leo in the papal library.

The visit comes at a delicate time for Charles following new revelations about his brother Prince Andrew, who is mired in a scandal surrounding late US sex offender Jeffrey Epstein.

Andrew announced on Friday he would relinquish his title as Duke of York, reportedly under pressure from Charles. He had already stepped back from royal duties in 2019.

The break with Rome created a schism that remains to this day, even if there has been a significant rapprochement in recent decades.

In 1961, the late Queen Elizabeth II, Charles's mother, became the first British monarch to visit the Holy See since the split.

The law was changed in 2013 so that marrying a Catholic would no longer disqualify someone from becoming monarch -- although they still have to be a Protestant themselves.

The rapprochement is important because "Anglicanism was born in reaction to the Catholic Church, and therefore in opposition," said Hyacinthe Destivelle, a French priest and member of the Vatican's dicastery (department) for promoting Christian unity.

This is no longer the case, despite "theological differences in recent decades", he told AFP.

Unlike the Roman Catholic Church, the Church of England -- the mother church of the world's 85-million-strong Anglican community --  ordains women and allows priests to marry. 

Sarah Mullally was recently named the first woman Archbishop of Canterbury, the Church's top cleric, although she has yet to officially take up her post.

Charles and Camilla are also set to take part in a service at the Basilica of Saint Paul Outside the Walls in Rome, one of four major papal basilicas, which has historic links with the English crown.

The king will be made a "Royal Confrater" of the basilica and presented with a specially designed seat for use by him and future British monarchs.

Charles has visited the Vatican several times and met privately with Pope Francis on April 9, just days before the pontiff's death.

The king sent his son and heir William to the funeral and his brother Prince Edward, the Duke of Edinburgh, to Leo's inauguration mass.

The visit comes as the Catholic Church celebrates the Jubilee, a year-long event held every 25 years which has drawn millions of pilgrims to the Vatican.