Zhukova was born as Darya Alexandrovna Zhukova in Moscow on 8 June 1981. Her father is Alexander Zhukov, an oil trader. Her mother is Yelena Zhukova, a Russian scientist of molecular biology. Her parents separated when she was 3. In 1991, she moved with her mother to the United States, settling in the Houston area as her mother had relocated due to work. They later moved to Los Angeles, California. Elena was then offered an opportunity at UCLA. By the time Elena retired, she was a professor of molecular biology there, as well as an authority on diabetes.
Zhukova attended a Jewish day-school in California. It was a Hebrew college, Dasha's first school in the US, and she attended it for three years. She attended Pacific Hills School, graduating in 1999. She graduated with honors from the University of California, Santa Barbara with degrees in Slavic studies and literature. After becoming involved with Roman Abramovich, she returned to Moscow and later moved to London, where she entered London's College of Naturopathic Medicine. She did not complete the program.
Zhukova co-founded the fashion label Kova & T in 2006. She sits on the board of the Los Angeles County Museum of Art (LACMA), an organization to which she has contributed.
In 2008, Zhukova founded the Garage Center for Contemporary Culture (part-funded by Abramovich) in Moscow, a nonprofit organization supporting the advancement of contemporary art and culture in Russia and abroad. In 2012, the Center launched the first comprehensive art education program and public archive of Russian art in the country. In 2014, the institution changed its name to Garage Museum of Contemporary Art and, the following year, moved to its first permanent home in Gorky Park. The building, designed by Rem Koolhaas, is a preservation project that transformed a 1968 Soviet Modernist restaurant into a radical space for exhibitions, publishing, research, and education.
Zhukova is the creative director of New Holland Island in St. Petersburg, overseeing the commercial and architectural development of the eight-acre island in the heart of the city. The island, created by Peter the Great, has lain vacant for almost 300 years. Known now as "art island", the development will include cultural spaces, as well as commercial and residential property.
In February 2009, Zhukova was appointed editor-in-chief of the fashion magazine Pop. Many in the industry saw her as an unlikely replacement for launch editor Katie Grand. In an interview at the time she was unable to name a single artist she admired, saying she was bad with names. She resigned from the position after three issues in November 2010.
In addition, Zhukova is the editor-in-chief of GARAGE magazine, a biannual print publication that focuses on the collaboration between contemporary art and fashion. Since its inception, GARAGE magazine has worked with some of the world's most celebrated creators, and initiated global artistic dialogues. Among the magazine's contributors are artists such as Jeff Koons, Damien Hirst, Nick Knight, Marc Jacobs, Richard Prince, John Baldessari, Inez & Vinoodh, and Patrick Demarchelier. The magazine took its name and spirit from Garage Museum of Contemporary Art. She also is a founding member of the Culture Shed in New York.
In 2014, a photograph of Zhukova sitting on a chair designed as a mannequin of a black woman was featured on Buro 24/7, an online fashion publication. The photograph was widely criticized as racist. Buro 24/7 cropped the chair from the photo and Zhukova apologised, describing the chair as artwork and as "commentary on gender and racial politics". Zhukova added, "I utterly abhor racism and would like to apologise to those offended by my participation in this shoot".
Zhukova became a good friend of Ivanka Trump and was invited to the Trump Inauguration by her in January of 2017. This raised eyebrows since her husband, Roman Abramovich, is in Putin's inner circle and served as another connection between Trump and Putin.
In a 2008 secret ceremony, Zhukova married Roman Abramovich, a Russian oligarch and the main owner of the private investment company Millhouse LLC. The couple have two children, a son and daughter, who were both born in the USA. In August 2017 the couple announced that they would separate.