The relationship between Camilla and the Prince Charles, Prince of Wales began when they met at a polo match in 1970. Though she became one of the numerous girlfriends of Charles, and he was said to have wanted to marry her, Camilla was seen by royal courtiers as an unsuitable match for the future king. Charles had met Camilla too early, and that he had not asked her to wait for him when he went overseas for military duties in 1972.

In the 1970s, Camilla's sister, Annabel, worked as an artist in New York City. At the same time, Charles was acting as Colonel-in-Chief of the Royal Regiment of Wales, and would annually visit the regiment in New York, where he met Annabel. Camilla was also known to have visited her sister in New York during this period. It was thus said by some that it was then that the couple resumed their relationship, and that it continued throughout the Prince's engagement. In fact, at one point Lady Diana Spencer is said to have been snuck aboard the Royal Train for an intimate evening, when in reality, it was years later proven to have been Camilla. Prince Charles bulter, Stephen Barry, confirmed an intimate meeting between the two on the night before Charles' wedding to Diana. However, though the timing of these tangled relationships has been much discussed and dissected, reliable published reports indicate that they renewed their romantic relationship in the early 1980s.

The affair became public knowledge a decade later, with the publication of Diana: Her True Story, followed by the Camillagate scandal, wherein an intimate telephone conversation between Camilla and Charles was secretly recorded and the transcripts published in the tabloids. With the extra-marital relationship in the open, Diana gave a interview on the BBC programme Panorama, in which she blamed the relationship between Camilla, whom she privately referred to as the Rottweiler, and the Prince of Wales as the reason for the break up of her own marriage, saying: "Well, there were three of us in this marriage, so it was a bit crowded." Though Camilla kept a low profile at this time, she became unpopular by these revelations, which her friends denied, suggesting that everything was a tabloid media invention that had become an urban myth. However, it was confirmed by Charles in a televised interview with Jonathan Dimbleby that the relationship between him and Camilla resumed during their respective marriages. Following this, the Parker Bowleses, whom had been living apart for some time, announced their own divorce in 1995.

Camilla occasionally became Charles' unofficial companion at events. This temporarily ceased at the time of Diana's death, but Camilla and Charles were photographed in public together in 1999, following a birthday party for Parker-Bowles's sister, Annabel Elliott. Though she maintained her residence in Wiltshire, Camilla then moved into Charles' household in 2003, resulting in decorative changes to both homes, though Buckingham Palace was explicit in pointing out that public funds had not been used for the renovations. In 2005, the media reported that Charles had also bought Camilla jewellery and a designer wardrobe. Marriage between the couple remained elusive, however: As the future Supreme Governor of the Church of England, the prospect of Charles marrying a divorcée was seen as controversial. Opinion – of both the public and the church – shifted, though, to a point where civil marriage was seen as an agreeable solution

On 10 February 2005, it was announced by Clarence House that Camilla and the Prince of Wales were engaged; Camilla had been presented with an engagement ring that had belonged to the late Queen Elizabeth, the Queen Mother. The marriage was to have been on 8 April of that year, and was to take place in a civil ceremony at Windsor Castle, with a subsequent religious blessing at St George's Chapel. But, because the conduct of a civil marriage at Windsor Castle would oblige the venue to thereafter be available to anyone wishing to be married there, the location was changed to the Windsor Guildhall. On 4 April it was announced that the marriage would be delayed by one day to allow for the Prince of Wales and some of the invited dignitaries to attend the funeral of Pope John Paul II. As Charles' parents did not attend the marriage ceremony (the Queen's reluctance to attend arising from her position as Supreme Governor of the Church of England), neither did Camilla's father; her children, instead, acted as witnesses of the union, as did Prince William and Prince Harry. The Queen and Duke of Edinburgh did, however, attend the service of blessing, and held a reception for the newlyweds at Windsor Castle afterwards. Following the wedding, the couple travelled to the Prince's country home in Scotland, Birkhall, and carried out their first public duties as a couple during their honeymoon.