She joined the Royal Ballet (then called the Sadler's Wells Theatre) while still a teenager, after having been trained by some of the greatest teachers of the day - Olga Preobrajenskaya and Mathilde Kschessinskaya, both of whom trained under Marius Petipa himself. By 1939, she was the company's star and the inspiration for many of Sir Frederick Ashton's ballets, such as Undine, Daphnis and Chloe, and Sylvia. She was especially renowned for her portrayal of Aurora in Tchaikovsky's Sleeping Beauty. Televised versions of Sleeping Beauty and Ashton's version of Cinderella are now available on DVD. Fonteyn also worked with the choreographer Roland Petit and later in life, Martha Graham. In 1949, the Royal Ballet toured the United States and Fonteyn became an instant celebrity.
Ashton choreographed Marguerite and Armand for them, which no other couple danced until the 21st century. They debuted Kenneth MacMillan's Romeo and Juliet, although MacMillan had conceived the ballet for Lynn Seymour and Christopher Gable. Fonteyn and Nureyev appeared together in a film version of Swan Lake and Kenneth MacMillan's Romeo and Juliet, as well as Les Sylphides and the Le Corsaire Pas de Deux.
Despite their differences in background, temperament, and a nineteen-year difference in age, Nureyev and Fonteyn became close lifelong friends and were famously loyal to each other. Fonteyn would not approve an unflattering photograph of Nureyev. He 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."The extent of their physical consummation remains unclear - Nureyev said that they had a physical relationship while Fonteyn denied it; her biographer agrees with Nureyev's version. In 1967, they were arrested after a performance in San Francisco, when the police raided a Haight-Ashbury party to which they had been invited. They remained close even after she retired to a Panama cattle farm, talking on the phone several times a week even though her farmhouse did not have a telephone. When she was treated for cancer, Nureyev paid many of her medical bills and visited her often, despite his busy schedule as a performer and choreographer, as well as his own health problems (he was HIV positive and succumbed to AIDS in 1993). In a documentary about Fonteyn, Nureyev said that they danced with "one body, one soul" and that Margot was "all he had, only her." An observer said that "If most people are at level A, they were at level Z."
In the extremely competitive world of ballet, Fonteyn was renowned for her consummate professionalism and loyalty to her friends. Her dancing stood out for its lyricism, grace, and passion. Although Fonteyn was the Royal Ballet's biggest star, its director, Dame Ninette de Valois, cultivated other talents, so that the Royal Ballet of Fonteyn's day also included Nadia Nerina, Svetlana Beriosova, Lynn Seymour, and Antoinette Sibley.
The cost of his medical care is a reason why Fonteyn's career lasted until 1979, her sixtieth year, despite her suffering from an arthritic foot. Upon her retirement, the Royal Ballet honoured her with the title prima ballerina assoluta. She ended her days in Panama, remaining loyal to Arias in part because she was very devoted to his children from an earlier marriage. Because Arias's medical bills drained her finances, the Royal Ballet held a special "gala" in 1990 for her benefit. Shortly after his death, she was diagnosed with a cancer that proved fatal.
A dramatic image of her performing Swan Lake at the Bath Festival, Bath, United Kingdom, was captured by British photographer Des Gershon, taken secretly from the high gallery of the Theatre Royal, Bath, as she danced with the corps de ballet on the day she heard that there had been an assassination attempt on the life of her husband. The stress, worry and pain is clearly shown in her face with the remarkable single frame of a moment in time. View the image here
She was chancellor of the University of Durham from 1981 to 1990. The main hall in Dunelm House, the Student Union building, is named the Fonteyn Ballroom in her honour.
There is a school dedicated to Margot Fonteyn that bears her name. The Margot Fonteyn Academy is located just north of New York City (Peekskill) and was founded by her close friend Ken Ludden who teaches the classical style of ballet favored by Dame Margot.
Fonteyn envisioned an international fine arts institution in which all of the arts would be studied under one roof. Her belief was that young artists of divergent fields of expression would enter into conversations about the core issues of art (expression, interpretation, focus, et cetera), and would consequently develop a deeper understanding of the artistic purpose of their endeavors. She and Ludden worked together to develop this concept for the last twelve years of her life.
"I do think it would be good to have artists studying side by side in the different disciplines instead of each group isolated in its own world....the objective would be to produce professional artists integrated from their school days with exponents of the sister arts. Many benefits would ensue, especially for ballet itself which is a composite of the four arts. The ideal would be Music, Dancing, (principally ballet and ballet related dancing), Painting and Drama. Those four are the basic elements of theatre." --Dame Margot Fonteyn d'Arias (from correspondence with Ludden)