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France's Stephanie Frappart, Salima Mukansanga of Rwanda and Japan's Yoshimi Yamashita are among the 36 referees to have been selected by the world governing body.
In total, there are six female officials among the 129 referees, assistant referees and VARs announced on Thursday, also including assistants Neuza Back from Brazil, Karen Diaz Medina from Mexico and Kathryn Nesbitt from the USA.
"This concludes a long process that began several years ago with the deployment of female referees at FIFA men’s junior and senior tournaments," said legendary Italian referee Pierluigi Collina, now the chairman of FIFA's referees' committee.
"In this way, we clearly emphasise that it is quality that counts for us and not gender. I would hope that in the future, the selection of elite women’s match officials for important men’s competitions will be perceived as something normal and no longer as sensational. They deserve to be at the FIFA World Cup because they constantly perform at a really high level, and that’s the important factor for us."
Frappart has already made history as the first woman to have refereed a Ligue 1 match, a Champions League match and a World Cup qualifier, and officiate at a European Championship acting as a fourth official for last summer's tournament.
The 38-year-old also refereed the 2019 Super Cup final between Liverpool and Chelsea, which Liverpool won on penalties.
Anthony Taylor and Michael Oliver will be the Premier League's representatives in Qatar, having both made their big tournament debuts at the Euros.