stylistic:tone, quality:correction
Nureyev years (1961–1979)

Fonteyn began her greatest artistic partnership at a time when many people, including the head of the Royal Ballet, Ninette de Valois, thought she was about to retire. In 1961 Rudolf Nureyev, star of the Kirov Ballet, defected in Paris and was invited by de Valois to join the Royal Ballet. She offered Fonteyn the opportunity to dance with him in his debut, and though reluctant because of their 19-year age difference, Fonteyn agreed. On 21 February 1962, Nureyev and Fonteyn performed together in Giselle to an enthusiastic capacity crowd, for which they received 15 minutes of applause and 20 curtain calls. The performance was followed by a show-stopping performance of Le Corsaire Pas de Deux on 3 November. The press described their performance as "otherworldly"; The Observer called it a "knockout" and the pairing "history-making". A few days later, they performed Les Sylphides to rave reviews, which were carried in United States newspapers. Fonteyn was awarded an honorary Doctor of Laws from the University of Cambridge in 1962.

Sir Frederick Ashton choreographed Marguerite and Armand for them, which no other couple danced until the 21st century. The 1963 premiere was well publicised before its opening and teamed them with Michael Somes, who played the disapproving father. Composed as a series of pas de deux, interrupted by only one solo, the ballet built intensity from the initial coup de foudre to the death scene. According to Somes, the pairing of Nureyev and Fonteyn was brilliant, as they were not partners but two stars of equal talent who pushed each other to their best performances. Attended by the Queen Mother, Princess Margaret and Princess Marina, the production was an immediate success. It became a signature work for the duo, sealing their partnership.

In 1964, Fonteyn and Nureyev toured from Sydney to Melbourne, performing in Giselle and Swan Lake with The Australian Ballet. After a brief break, they resumed their performances in Stuttgart. On 8 June that year, while the duo were performing in Bath, they were advised that a rival Panamanian politician had shot Fonteyn's husband Arias, but it was unclear if he was in imminent danger. Fonteyn, though shaken, danced in MacMillan's new pas de deux, Divertimento, on 9 June, before flying home to Panama. She found that Arias had been shot four times by Alfredo Jimenez, leaving him a quadriplegic for the rest of his life. Thoughts of retirement receded, as she needed to continue working to pay Arias' medical bills. Though he used a wheelchair, Fonteyn took him with her on most of her travels. Within two weeks, she had returned to London, having arranged for Arias to be treated at the National Spinal Injuries Centre of the Stoke Mandeville Hospital, and resumed dancing. Over the next ten days, Fonteyn danced in six performances of La Bayadère, Giselle, and Marguerite and Armand while rehearsing Nureyev's production of Raymonda. A coma and relapse in Arias' condition forced her to miss all but the final performance of Raymonda in Spoleto.

Fonteyn and Nureyev were especially noted for their performance of classics, such as The Sleeping Beauty and Swan Lake, which Fonteyn stripped to the essence of the roles and constantly improved her performance. Nureyev insisted that Fonteyn partner with him in La Bayadère and Raymonda, and wrote his own version of Swan Lake for them to perform with the Vienna State Opera Ballet in 1964. The performance was filmed and Lord Snowdon took pictures for the 27 November 1964 issue of Life. On 20 January 1965, Fonteyn and Nureyev performed the Le Corsaire Pas de Deux at the inaugural ceremonies for President Lyndon B. Johnson in Washington, D. C. Later that year, the couple debuted the title roles in Romeo and Juliet choreographed by Sir Kenneth MacMillan. MacMillan had intended the roles to be performed by Lynn Seymour and Christopher Gable, but David Webster, the manager of the Royal Opera House, insisted on Fonteyn and Nureyev. A year after the debut, the production was still drawing queues for its nightly performances. The audiences littered the duo with flowers, demanding repeated curtain-calls. Fonteyn's depth as an actor made the performance unique, making Juliet one of her most acclaimed roles.

Despite differences in background and temperament – she was methodical while he was wildly exuberant – and a 19-year gap in their ages, Fonteyn and Nureyev became lifelong friends and were famously loyal to each other. Fonteyn would not approve an unflattering photograph of Nureyev, nor would she dance with other partners in ballets within his repertoire. The extent of their physical relationship remains unclear; Nureyev said that they had one, while Fonteyn denied it. Her biographer, Meredith Daneman, said that in spite of no real evidence, her opinion was that they did, yet Nureyev's biographer, Diane Solway concluded that they did not. Nureyev said about her:

"At the end of 'Lac des Cygnes', when she left the stage in her great white tutu I would have followed her to the end of the world."

In 1965, Fonteyn and Nureyev appeared together in the recorded versions Les Sylphides, and the Le Corsaire Pas de Deux, as part of the documentary An Evening with the Royal Ballet. The film grossed over US$1 million, creating a record for a dance film at the time, and was shown in over 50 theatres in New York and New Jersey alone over the week of 6 December 1965. Under the guidance of director Paul Czinner, who used a multi-camera technique to give the feel of a stage performance, they also filmed their famous version of Romeo and Juliet in 1966. That same year, she was awarded an honorary doctorate of music by the Duke of Devonshire upon his installation as the Chancellor of the University of Manchester. In 1967 Roland Petit wrote a new ballet for the duo, Paradise Lost. It was an abstract, modern production designed to emphasize Rudolf as a virile Adam and Fonteyn as a chic Eve. With pop art décor and flashing neon, the ballet titillated the fans, including Mick Jagger and his girlfriend, the singer Marianne Faithfull.

Fonteyn went into semi-retirement in 1972, relinquishing parts in full ballets and limiting herself to only a variety of one-act performances. In 1974, she was awarded the Royal Society of Arts ' Benjamin Franklin Medal, in recognition of her having built bridges between Britain and the U.S. through her art. She ventured into modern dance, performing as "Desdemona" in José Limón ' The Moor's Pavane June 1975 with the Chicago Ballet followed by a performance of the same dance with Nureyev at The Kennedy Center in Washington, D.C., in July. Between the two performances, Fonteyn was appearing with the Martha Graham Dance Company in Saratoga, New York City, Athens and London. After the performance at The Kennedy Center, her tour went on to Brazil. In November 1975, she and Nureyev appeared in Fonteyn & Nureyev on Broadway at the Uris Theatre. The appearance, though memorable, confirmed that Fonteyn was no longer able to execute more demanding roles. In 1976, she published her autobiography, though it was not a tell-all. Her husband was still living and Fonteyn was a very private person, as well as proper and fastidious. In 1977, she was awarded the Shakespeare Prize, in Hamburg by the Alfred Toepfer Stiftung F.V.S., as the first dancer ever honoured with the award.