The King has become the first British monarch to pray in a public service with the Pope since the Reformation five centuries ago.
Marking an extraordinary moment in religious history, Charles, Supreme Governor of the Church of England, prayed with Pope Leo XIV, head of the Catholic Church, during an ecumenical service in the famous Sistine Chapel on Thursday.
The Archbishop of York also attended the service in the Sistine Chapel, as did Foreign Secretary Yvette Cooper, who stood to deliver a Bible verse from a Letter to the Romans, written by St Paul.
Pope Leo marked the end of the service by reading a prayer. He read: “God our father, you created the heavens and the earth. You made us in your image. Teach us to see your hand in all your works and your likeness in all your children.”
The King and Pope then left the Sistine Chapel, where the Queen remained to meet the choirs.
Earlier, Charles and Camilla met the Pope for a private reception at the Vatican as the couple began their historic two-day state visit.
The visit to the Holy See, the government of the Roman Catholic Church in the Vatican, is understood to be deeply significant for the King personally and will celebrate the Papal Jubilee which is celebrated every 25 years. It also marks the first time the monarch has met with Pope Leo since he was elected to the position in May.
The King and Queen's official limousine drove through St. Peter's Square on Thursday morning, where crowds traditionally gather to see the Pope, and headed to the Courtyard of St. Damasus, the ceremonial entrance to the Apostolic Palace, the pontiff's official residence.
Waiting to receive them was the Reverend Monsignor Leonardo Sapienza, Regent of the Prefecture of the Papal Household, and an honor guard provided by the Vatican's famous Swiss Guard. The guard, made up of Catholic Swiss citizens, has protected the head of the Catholic Church for centuries.
The royal couple stood as the national anthems of Britain and Vatican City were played. They also met a group of Papal Knights.
After the welcoming ceremony, Monsignor Sapienza led the King and Queen to the Apostolic Palace to meet with Pope Leo, ahead of a historic day of events.
Later, the Kings will attend a religious service in the Basilica of Saint Paul Outside the Walls, where a special seat has been created for Charles, which will remain in the place of worship for the use of his successors.
Charles will also be recognized for the British monarchy's historical association with the basilica, the seat of a Benedictine abbey, and will be made a “royal brotherhood” of the abbey as, in centuries past, monarchs were responsible for the upkeep of St Paul's tomb in the basilica.
The state visit will end with the King attending a reception at the Pontifical Bede College, a seminary that trains priests from across the Commonwealth, and the Queen will meet six Catholic sisters from the International Union of Superiors General.
The Queen wore a traditional black dress to meet Pope Leo on Thursday morning, including a veil over her head and shoulders. Her silk dress was by Fiona Clare, the mantilla or veil was made by milliner Philip Treacy, and she wore the late Queen's “raspberry seed” brooch in the shape of a cross.
The King and Queen were due to make a state visit to the Holy See in April, but Pope Francis' health problems meant the trip was postponed, although the couple met privately with the pontiff, who died that same month.
The King also met with two of Pope Leo's predecessors: Pope Benedict XVI and Pope John Paul II.
