Anna Wintour is stepping down as editor in chief of the American edition of Vogue after more than three decades atop the fashion magazine, setting the stage for a younger editor to help shape the iconic publication.

During her 37-year tenure, Wintour ran day-to-day operations of the American title and grew into a cultural tastemaker, building relationships with major fashion houses and elevating up-and-coming designers. Her face was a staple in the front row of fashion shows around the world, and she helped inspire Meryl Streep’s character in the film “The Devil Wears Prada.” She made the Met Gala one of fashion’s most high-profile events .

Wintour, 75 years old, will continue to serve as Condé Nast’s global chief content officer and global editorial director of Vogue. In her role as chief content officer, Wintour oversees much of Condé Nast’s portfolio, including Vanity Fair, Glamour, Allure and GQ.

The company plans to hire a new head of editorial content for American Vogue. Roger Lynch , chief executive of Condé Nast, said that Wintour had been doing three jobs since 2020 and that it made sense for her to step back from American Vogue at this time. “This will enable her to make time for everyone who needs her,” he said.

Vogue’s circulation for the six-month period ended Dec. 31 was about 1.2 million, including print and digital—essentially unchanged from the same six-month period in 2019—according to the Alliance for Audited Media.

The publication, however, has had an impact far beyond its circulation numbers. Its cover has been graced by musicians, actors and sports stars, as well as designers and other celebrities from Kim Kardashian to former first lady Jill Biden.

Wintour was awarded a Presidential Medal of Freedom earlier this year .

“To me, it feels that she’ll still be very much involved,” said Tina Brown , the former editor of Vanity Fair and the New Yorker. “Being in charge of all their brands while micromanaging one magazine is a lot. This makes absolute sense.”

Write to Isabella Simonetti at isabella.simonetti@wsj.com and Jeffrey A. Trachtenberg at Jeffrey.Trachtenberg@wsj.com