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Born in Buenos Aires to a Scottish father and American mother, Agar moved with her family to London in 1911. Her father was the head of a family business selling windmills and other agricultural machinery to Argentina. At a young age, Agar became fascinated by pictures by Edmund Dulac and Arthur Rackham. Before attending school, Agar grew up in her family villa Quinta la Lila learning from her nanny and a French governess. Agar describes her childhood as being "full of balloons, hoops and St Bernard dogs". The family travelled to Britain approximately every two years during her childhood. Aged six Agar was sent to England to a private school in Canford Cliffs. At her second school, Heathfield School, Ascot, Agar's teacher Lucy Kemp-Welch encouraged her to continue to develop her art. In 1914 at the onset of World War I Agar was sent away to Tudor Hall from her home in London to avoid the hardships of war. In Kent the music master Horace Kesteven began introducing her to various artists. Through Kesteven, Agar met Charles Sims who exposed her to some of Paul Nash's early works. Agar describes her time with Sims as "I found myself in a milieu of art where art was a valued part of daily life".

Before the war ended, Agar attended the Demoiselles Ozanne to improve her French and while she was there she took weekly oil painting lessons at the Byam Shaw School of Art in Kensington. Agar found the Byam Shaw too academic and pleaded with her family to allow her to look elsewhere to continue her schooling. This infuriated her mother and after an argument with her parents Agar notes in her diary that she got up early, ate lunch with her sisters, and packed her bags and departed from Paddington Station. She left a note for her parents stating that she was on her way to Truro and St Mawes where she would stay with a family friend the De Kays.

Then, from 1920-1, she studied under Leon Underwood at his school at Brook Green. There she made friends with Blair Hughes-Stanton and Gertrude Hermes, amongst others. She studied part-time under the legendary Henry Tonks at the Slade School of Fine Art in London from 1921 to 1924, alongside Rex Whistler and Cecil Beaton, and her first husband - Robin Bartlett. With him and others, Agar travelled around France and Spain. In 1925 she married Bartlett, the year that she destroyed the majority of her early work. The pair lived together in a house in Dieppe. Agar described him as "the escape-hatch which freed me from the clutches of my family". In 1926, Agar met the Hungarian Joseph Bard, the man with whom she would spend the next 50 years, and whose passion for jewels she would integrate into her practice.

Between 1927 and 1928, Agar and Bard lived in London, and in Portofino in the winter, where Agar met Ezra Pound, who was to become a friend. 1928, Agar and Bard moved to Paris, where she met the Surrealists André Breton and Paul Éluard, with whom she had a friendly relationship. In the period 1928-30, Agar studied with the Czech cubist, František Foltýn. With Pound, Agar visited Constantin Brâncuși' s studio.

In 1930, Agar returned to England, and painted her first surrealist piece, The Flying Pillar, based on André Breton's surrealist manifesto. Agar describes her piece in her memoir as "her first attempt at an imaginative approach to painting and although the result was surreal, it was not done with that intention". Agar said that "Surrealism was in the air in France and poets in France, later in England, were kissing that sleeping beauty troubled by nightmares, and it was the kiss of life that they gave". The Flying Pillar was later renamed the Three Symbols, and is described by Agar as a reference both to Greek art and to Gustave Eiffel and his famous tower, the symbol of modernity. The painting represented the classical world merging with the modern at a crossroads in time. She describes the various images in her painting in her 1928 diary entry as Greece being the meeting place of Judaeo-Egyptian and Greco-Christian followed by the words "'the Judaeo-Graeco pillar' as if it were a note to bear in mind and to later be developed".

In 1931, the first of four issues of The Island was published, edited by Leon Underwood and Joseph Bard. Agar contributed to all four issues. Two years later she had her first solo show at the Bloomsbury Gallery. She was a member of the London Group from 1934 onwards - in the same year, she made her first collage.

In 1934, Agar and Bard took a house for the summer at Swanage, Dorset. Here she met Paul Nash and the two began an intense artistic and sexual relationship. In 1935 Nash introduced Agar to the concept of the found object. Together, they collaborated on a number of works, such as Seashore Monster at Swanage. Nash recommended her work to Roland Penrose and Herbert Read, the organisers of the 1936 London International Surrealist Exhibition at the New Burlington Galleries, despite Agar's denial of the moniker of Surrealist throughout her life. She was one of only a very few women included in the exhibition. Agar exhibited with the Surrealists in England and abroad. During the 1930s Agar's work focused on natural objects often in a light-hearted manner such as Bum-Thumb Rock, a set of photographs of an unusual rock formation she noticed in Brittany. She started to experiment with automatic techniques and new materials, taking photographs and making collages and objects. The Angel of Anarchy, a plaster head covered in fabric and other media, is such an example from 1936–40 and is now in the Tate collection. She created two versions of The Angel of Anarchy after her first Angel of Anarchy was lost on its way back from a show in Amsterdam. She made her second version in 1940 using the same cast of Joseph Bard's head and kept the original title The Angel of Anarchy. The bust was divided into two parts, one with white fur and one with black fur, with most of the head covered in green osprey and ostrich feathers and dollies that she received from her mother who used to wear them as a head dress.

In 1937, Éluard visited Agar and Bard in London, travelled down to Cornwall with Nusch Éluard, Roland Penrose and Lee Miller, and begun an affair with Paul Éluard. She visited Picasso and Dora Maar's home in Mougins, Alpes-Maritimes, along with Lee Miller, who photographed her. By 1940, works by Agar had appeared in surrealist exhibitions in Amsterdam, New York, Paris and Tokyo. "The war interrupted her artistic activity, and she only began to paint again in 1946 and exhibited fairly regularly from then on until her death."

After World War Two, Agar started a new productive phase of her life, holding almost 16 solo exhibitions between 1946 and 1985. By the 1960s she was producing Tachist paintings with Surrealist elements. In 1988 she published her autobiography A Look At My Life. then in 1990, she was elected as a Royal Academy Associate. She died in London. Agar has paintings in the collection of several British institutions including Tate, Derby Art Gallery, Bradford and the UK Government collection.

Eileen Agar is buried in the Pere Lachaise Cemetery, Paris. Grave No. 17606. Goshka Macuga's 2007 exhibition, part of Tate Britain's Art Now Series, used material drawn from Eileen Agar's Archive.