King Charles and Queen Camilla received a papal blessing to mark their anniversary during a private audience with Pope Francis in April.
The special gesture was issued to mark the royal couple's twentieth wedding anniversary, according to fresh details from Robert Hardman's revised biography of the monarch.
The revelation appears in the updated edition of "Charles III" and sheds new light on the couple's meeting with the late pontiff at the Vatican.
The encounter, which lasted twenty minutes and took place behind closed doors, occurred despite the Catholic Church's position on remarriage after divorce.
Pope Francis blessed King Charles and Queen Camilla's anniversary during their last meeting
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Under Catholic doctrine, which does not recognise second marriages whilst former spouses remain living, the King and Queen's marriage would not be recognised as Andrew Parker Bowles, Camilla's ex-husband, still lives.
The meeting also marked a watershed moment in relations between the Church of England and Rome, The Telegraph reported.
Hardman revealed the King and Pope prayed together which would potentially be the first such prayer between a Supreme Governor of the Church of England and a pontiff since Henry VIII's break with the church in 1534.
"It might have been a short prayer, with the frail Pope in his chair and the King, alongside the Queen, on his feet. But it was a post-Henry VIII landmark," Hardman wrote.
The Pope blessed the royal couple despite the Catholic church's stance on remarriage after divorce
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The biographer noted that whilst the late Queen Elizabeth II encountered four popes during her reign, she never prayed alongside them.
At the time, the Vatican's formal statement acknowledged that "Pope Francis met privately with Their Majesties, King Charles and Queen Camilla".
They added that the Pope had: "Expressed his best wishes to Their Majesties on the occasion of their wedding anniversary."
Buckingham Palace responded that the royal couple were "deeply touched by the pope's kind remarks about their 20th wedding anniversary, and honoured to be able to share their best wishes with him in person."
Charles and the Pope are also believed to have prayed together, a watershed moment in relations between the Church of England and Rome
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Pope Francis died just 12 days following this historic encounter.
Following the death of Pope Francis, His Majesty the King has issued the following message: "My wife and I were most deeply saddened to learn of the death of Pope Francis.
"Our heavy hearts have been somewhat eased, however, to know that His Holiness was able to share an Easter Greeting with the Church and the world he served with such devotion throughout his life and ministry.
"His Holiness will be remembered for his compassion, his concern for the unity of the Church and for his tireless commitment to the common causes of all people of faith, and to those of goodwill who work for the benefit of others. His belief that care for Creation is an existential expression of faith in God resounded with so many across the world.
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Prince William represented the King at the funeral mass of Pope Francis
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"Through his work and care for both people and planet, he profoundly touched the lives of so many.
"The Queen and I remember with particular affection our meetings with His Holiness over the years and we were greatly moved to have been able to visit him earlier in the month.
"We send our most heartfelt condolences and profound sympathy to the Church he served with such resolve and to the countless people around the world who, inspired by his life, will be mourning the devastating loss of this faithful follower of Jesus Christ."
The King signed the message: "Charles R."
Prince William represented the King at the funeral mass of Pope Francis.