Wales Bonner, who was born in London to an English mother and Jamaican father, founded her own label in 2014, not long after graduating from London's Central Saint Martins College of Art.
According to Vogue, Wales Bonner will continue her namesake brand alongside her new Hermès role.
She dressed F1 driver Lewis Hamilton, musician FKA Twigs, and actor Jeff Goldblum for this year's Met Gala and has made T-shirts with musician Solange Knowles, younger sister of Beyoncé.
Wales Bonner has also curated an exhibition at the Museum of Modern Art in New York and hosted musical performances at London's Serpentine Galleries.
She has had a long-standing collaboration with Adidas and was made a MBE in 2022 for services to fashion.
Pierre-Alexis Dumas, general artistic director of Hermès, said: "I am really pleased to welcome Grace to the Hermès artistic director family.
"Her take on contemporary fashion, craft and culture will contribute to shaping Hermès men's style, melding the house's heritage with a confident look on the now.
"Grace's appetite and curiosity for artistic practice strongly resonate with Hermès's creative mindset and approach. We are at the start of an enriching mutual dialogue."