Dressed in a fitted white basque, the 65-year-old revealed her new name is Caitlyn.
Jenner also set up a verified Twitter account under the name Caitlyn, where she tweeted, "I'm so happy after such a long struggle to be living my true self."
"Welcome to the world, Caitlyn. Can't wait for you to get to know her/me."
Vanity Fair launched the hashtag #CallMeCaitlyn, spurring a wave of positive messages about Jenner who broke records in the decathlon nearly 40 years ago.
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Kim Kardashian, Jenner's stepdaughter, voiced admiration over the Vanity Fair photographs, tweeting "How beautiful! Be happy, be proud, live life YOUR way!"
Speaking to Vanity Fair, Jenner said she had struggled at stages of her transition to a woman to accept her choices.
Following facial surgery to feminise her features, Jenner says she woke up panicked.
"What did I just do? What did I just do to myself?" she says she asked.
But after speaking with a counselor, Jenner says she realised the reaction was normal.
The cover portrait, by renowned photographer Annie Leibovitz, was taken in Jenner’s Malibu, California home for Vanity Fair’s July issue. The accompanying 22-page article reveals that Jenner underwent 10 hours of facial-feminization surgery in March, but has not yet opted for sex reassignment surgery.
In addition to the cover photo, Jenner appears in Vanity Fair wearing a variety of high-fashion styles that play up her femininity. In one image, she takes the wheel of a black sports car wearing a tight crimson dress, while in another she wears a lacy corset under a motorcycle jacket.
Jenner, 65, became the most high-profile American to identify as transgender, making the announcement in an interview with ABC's Diane Sawyer in April.
Jenner, who has been prominently featured as the patriarch on E! Entertainment’s "Keeping Up with the Kardashians," will star in an E! documentary this July chronicling her new life as a woman.
ESPN announced Monday that it will grant Jenner the Arthur Ashe Courage Award, given to "individuals whose contributions transcend sports," at the Excellence in Sports Performance Yearly Award ceremony in July.
