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Muguruza, 22, is the first Spanish women’s champion at Roland Garros since Arantxa Sanchez Vicario in 1998.
Twelve years younger than the veteran American, and playing in the first clay court final of her career, the Venezuelan-born Spaniard upset the odds to win 7-5, 6-4.
“I am so excited to play the final of a Grand Slam against one of the best ever players. It’s the perfect final and I am so happy,” she said.
“Serena is a very powerful player and I just tried to fight as hard as I can.”
For Williams it was a second straight loss in a Grand Slam final and it wrecked her hopes once again of winning a 22nd Grand Slam title to draw level with German legend Steffi Graf.
She will now turn her focus on Wimbledon where she will be the defending champion and a six-time former winner.
Big serves, explosive groundstrokes
The players took contrasting routes to get to the final.
Fourth seed Muguruza breezed through, losing just one set in her opening match, while Williams struggled past the quarter- and semi-finals amid talk of an injury or illness.
But with weather conditions improving after one of the rainiest Roland Garros tournaments on record, it was a different, more focused Williams that got the final under way with a love service game.
Muguruza replied in kind as two of the biggest and best servers in the women’s game went head to head.
The Spaniard had to battle hard to level at 2-2, saving two break points along the way, but she then grabbed the first break of the final thanks to a loose game from the American culminating in a double fault.
Muguruza, who lost to Williams in the Wimbledon final last year, moved 4-2 ahead, but she lost her range two games later to allow the American to level the score.
The tall Spaniard was matching Williams for power and when the title-holder opened the 11th game with a double fault she seized the opportunity to apply some added pressure on her opponent.
Her tactics paid off with Williams failing to cope with a series of explosive baseline groundstrokes.
Muguruza’s second break of the final allowed her to serve for the set and she duly managed that, staving off two break-back points along the way.
Muguruza maintained her level of play and composure to start the second set with a third break of serve, but she then struggled on her own serve, coughing up a seventh double fault to hand back the advantage.
Scream of defiance
Williams though was struggling and this time it was the quality of her opponent’s play rather than her own misgivings that were responsible for her struggles.
Muguruza made it three straight breaks of serve in the next game and moved out into a 3-1 lead.
Williams dug deep to get back to 3-2 sparking a scream of defiance from a player who had been in 26 Grand Slam finals dating back to 1999 and lost just five of them.
But Muguruza was solid on her serve despite the occasional double fault and the Spaniard went 4-2 and then 5-3 up.
Williams saved four match points in the next game to stay alive, but Muguruza stayed calm to serve out for the biggest win of her fledgling career.