Friends say the relationship has endured because the two are true soulmates, sharing a passion for country pursuits, and because Camilla has the ability to make Charles laugh and deflate his occasional stuffiness.
It was their mutual enthusiasm for polo that first brought them together, in 1970, at a match at Windsor Great Park, and from the beginning Charles was captivated by Camilla's sense of humour.
She jokingly mentioned that her maternal great-great-grandmother, Alice Keppel, was the long-time mistress of Charles's great-great-grandfather, Edward VII.
The then Camilla Shand is said to have told the Prince: "My great-great-grandmother was your great-great-grandfather's mistress, so how about it?"
They grew close, but Charles was not ready for marriage, and in 1971, he joined the Navy. The relationship cooled as he spent long periods away at sea.
Camilla subsequently wed cavalry officer Andrew Parker Bowles in 1973 and had two children – Tom, born in 1974, and Laura, who is five years younger.
The couple picked up where they had left off in the late 70s, but the relationship cooled once again. Charles was looking for a bride, and a married mother-of-two could never be a suitable candidate.
Camilla approved of his choice of the young Lady Diana Spencer, and accompanied her to Ludlow Races in 1980, during the Royal courtship.
But Charles's feelings for Camilla had not abated. Diana believed he had a tryst with his old flame two days before their fairytale wedding, and her suspicions appeared to be confirmed by a gold bracelet he presented to Camilla just before the marriage which bore the letters F and G intertwined – a reference to their pet names for each other, Fred and Gladys.
Royal watchers believe the relationship blossomed after the birth of Prince Harry in 1984, a period when Charles and Diana were drifting apart.
By 1992, it was clear that it was serious, when the so-called "Camillagate" tape surfaced.
In the recording of a telephone conversation between the two, made in December 1989, Charles said: "I love you" to Camilla and added many other highly personal comments.
Camilla remained resolutely silent about the relationship, but Charles hinted at its depth in a 1994 interview with Jonathan Dimbleby, in which he said: "Mrs Parker Bowles is a great friend of mine... a friend for a very long time. She will continue to be a friend for a very long time."
When the Prince admitted he had committed adultery after his marriage to Diana had broken down, Camilla was widely assumed to be the other woman involved.
She was now recognised everywhere, and her comfortable, country-set life was turned upside-down.
Women threw bread rolls at her in a supermarket as she faced a public backlash. Camilla had become "the marriage-wrecker".
She and Andrew Parker Bowles, a former Silver Stick-in-Waiting to the Queen, divorced in 1995 and Camilla became a regular visitor to the Prince's Highgrove home.
In April 1997, Camilla took a tentative step into public life when she became patron of the National Osteoporosis Society. An official photograph was released to mark the occasion.
In July that year, Charles hosted a party for Camilla to celebrate her 50th birthday.
The idea of Charles and Camilla as a couple was gradually being officially introduced to the public, but Diana's death changed all that. A charity function at which they may have appeared together, was cancelled.
A new attempt at introducing Camilla to the public was made two years later, when she met Princes William and Harry for the first time, joining them in hosting a glittering 50th birthday party at Highgrove for Charles.
In recent years, she regularly accompanied Charles to Prince's Trust galas, and became accustomed to donning an evening gown and jewels and facing the media.
And then, in June 2001, Charles kissed Camilla in public for the first time, in an acknowledgement that the worst-kept secret in British public life was finally out in the open.