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-Jewish 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 enrolled at the London's College of Naturopathic Medicine but did not complete the program.

In 2006, Zhukova co-founded the fashion label Kova & T with her childhood friend Kristina ‘Tina’ Tang, daughter of Chinese Entrepreneur David Tang. She sits on the board of the Los Angeles County Museum of Art (LACMA), an organization to which she has contributed.

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 US. In August 2017 the couple announced that they would separate.

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 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".