Pupul Jayakar was born in 1915 at Etawah, in the state of Uttar Pradesh. Her father was a liberal intellectual and senior officer in the Indian Civil Service, while mother came from a Gujarati Brahmin family from Surat, where Pupul spent her yearly summer breaks. She had a sister, Nandini Mehta. Her father's work took the family to many parts of India, where she got the opportunity to absorb local crafts and traditions early on in life.

At the age eleven, she went to Banaras (Varanasi), where she studied to a school started by Annie Besant, theosophist who was also active in Indian freedom movement, subsequently he father got posted to Allahabad, where she first came in contact with Nehru family at age fifteen, as her father was a friend of Motilal Nehru. Subsequently she became friends with daughter of Jawaharlal Nehru, Indira Gandhi.

She attended Bedford College in London before graduating from the London School of Economics in 1936. On returning home she married Manmohan Jayakar, a barrister, and settled down in Bombay (now Mumbai).

After settling in Bombay she launched Toy Cart, an English-language children's magazine illustrated by noted painters, Jamini Roy and M.F. Hussain. She became politically involved after becoming assistant to Congress activist Mridula Sarabhaiin the Kasturba Trust in 1940, she was also appointed assistant secretary of women’s affairs in the National Planning Committee, then headed by Jawaharlal Nehru. In the late 1940s she became friends with J Krishnamurti and also became involved in the handloom industry. She established the Weavers' Service Centre, Besant Nagar, Chennai, under the aegis of of the Ministry of Textiles.

Early on, she came a close friend with Indira Gandhi who, on becoming prime minister in 1966, appointed Jayakar as her cultural adviser. She became the executive director and later chairman, of the Handicrafts and Handloom Corporation of India. From 1974 for three years she chaired the All India Handicrafts Board (HHEC).

She was behind the Festivals of India organized in London, Paris and America lasting several months in the early 1980s and the Apna Utsav ("Our Festivals") during the tenure of Rajiv Gandhi, to whom she was also a cultural adviser, and held the rank of Cabinet minister. In 1982, she was appointed vice-president of Indian Council for Cultural Relations (ICCR), and remained vice-chairman of the Indira Gandhi Memorial Trust (1985-1989), apart from prime minister's adviser on heritage and cultural resources. At the request of her friend Indira Gandhi, she would found the Indian National Trust for Art and Cultural Heritage in 1984. .

Pupul Jayakar was one of the enduring supporters of the Hungry Generation literary movement in Bengal, India and had helped the Hungryalists during their trial during 1961. She was active with the Krishnamurti Foundation in India until her death. She helped in the establishment of the Krishnamurti Foundation in India, U. S. A., England and some Latin American countries. She also played a great part in running the Rishi Valley School at Madanapalle, Chittoor District of Andhra Pradesh.

She inspired many a young girl to be named after her unique name, prominent among those is Mrs. Nandini Pushkar Trivedi née Miss Nandini Vyas, the famous educationist who runs a school for the rural children on Bhopal-Berasia Road, by the name of Brigadier Trivedi Memorial Academy. Her popular name is Pupul, so kept by her parents from Varanasi, who were greatly influenced by Mrs. Pupul Jayakar's work, and that of her sister Ms. Nandini Mehta. Both Pupul and Nandini settled down in Mumbai.

She married Manmohan Jayakar, a barrister, in 1937, who died in 1972. Her daughter Mrs. Radhika Herzberger was born in 1938, who now presides and runs the Rishi Valley School at Madanapalle, Sahyadri School at Rajgurunagar, Pune and Rajghat College, Varanasi and some other KFI schools. Kathak danseuse, Aditi Mangaldas is her niece.

She died in Mumbai, on 29 March 1997, after a brief illness.

Her best known books are her two biographies "J. Krishnamurti: A Biography" (1988) and "Indira Gandhi: An Intimate Biography" (1992). In the latter, Jayakar reveals that her close friend Indira Gandhi had personally expressed to her a premonition of her death in the wake of the Operation Bluestar incident [1].