Peyton-Jones studied painting at the Royal College of Art between 1975–78, but did not continue a career as a professional artist. Two of her works still hang in the Bank of England. After her education, she was briefly an art lecturer at the Edinburgh College of Art. In 1988 she became a curator at the Hayward Gallery.
In 1991, Peyton-Jones became the director of the Serpentine Galleries. In 1998, she oversaw a major refurbishment of the gallery . In 2000 she inaugurated the annual Serpentine Gallery Pavilion, a project that invites an architect who has previously never been commissioned to work in the United Kingdom to create a temporary structure at the Gallery. The first pavilion was designed by Dame Zaha Hadid. Subsequent pavilions have been designed by Ai Weiwei, Jean Nouvel, and Oscar Niemeyer.
In 2013 she oversaw the expansion of the Serpentine into a second building, the Serpentine Sackler Gallery. The Serpentine Sackler Gallery is located in a Grade-II listed building, which was originally used for gunpowder storage, and has an extension by the architect Zaha Hadid. In October 2015, Peyton-Jones announced her departure from her role at the Serpentine Galleries in summer 2016. .
Dame Julia announced she was stepping down from her post in the Serpentine in October 2015, planning to work independently in contemporary art and architecture, and embark on new projects. “I felt after 25 years this was a good time to hand over the reins to someone new” she said. At age 64, in January 2017, the birth of her first child, a daughter, Pia was announced
Peyton-Jones was appointed Officer of the Order of the British Empire (OBE) in the 2003 Birthday Honours for services to art and Dame Commander of the Order of the British Empire (DBE) in the 2016 Birthday Honours for services to the arts.
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