Venezuela-born Spaniard Muguruza romped to a 7-5, 6-0 victory, adding her second Grand Slam to the French Open title she won in 2016.
In the first women’s final played under the Centre Court roof at Wimbledon, Muguruza proved too strong for Venus, who was looking to win her sixth SW19 title.
But the 23-year-old was left blushing after causing laughs around Centre Court by admitting she grew up watching Williams, 37, play.
“I had the hardest match today against Venus,” Muguruza said. “She’s such an amazing player. I grew up watching her play… sorry!”
The crowd laughed, with Muguruza joining in nervously as Venus remained unmoved, statuesque, probably wishing she was anywhere else.
And Muguruza had the assembled media in stitches later in her press conference, when she was asked who she would prefer to dance with at the Wimbledon dinner, Roger Federer or Marin Cilic.
She paused perfectly before answering: “Roger!” to widespread laughter.
“I like Cilic, but I would like to see if Roger is elegant at dancing also,” she added.
Garbine Muguruza triumphed over Venus Williams to win her first Wimbledon title
Muguruza had a message for her absent coach Sam Sumyk, who missed the match as his wife is about to give birth.
“Here it is!” she exclaimed. “I want to thank my team who are here… this is not only me, this is all team work.
“Two years ago I lost in the final against Serena and she told me I was going to win.”
Muguruza posted a picture of her holding the Wimbledon trophy aloft on Twitter soon after the match, with the simple caption: “Yes!!!!”
The 6ft star celebrated with her team in the corridors at Wimbledon, her crowning triumph shared with the former King of Spain Juan Carlos 1 and Arantxa Sanchez-Vicario, a beaten Wimbledon finalist in 1995 and 1996.
“Everyone is looking at me!” she laughed as she met the establishment and tennis royalty.
Her win was heralded as a big moment for Spanish tennis by Rafael Nadal, who crashed out in the first week.
“Congratulations @GarbiMuguruza champion @Wimbledon! Great success for the Spanish tennis!” he wrote.
Garbine Muguruza lost the 2015 Wimbledon final to Serena Williams
Venus Williams was chasing her first Wimbledon title since 2008
But for Venus, this was no laughing matter.
She only won 12 points in the second set against Muguruza and the 6-0 score was her first set lost to love at Wimbledon ever.
Venus put on a brave face on Centre Court as she chatted to Sue Barker, admitting she was missing her sister Serena.
Serena was not at Wimbledon this year because she is pregnant, allowing her older sis the chance to shine.
But unlike Serena in the 2015 Wimbledon final, Venus could not cope with Muguruza, but found time to send a message back home.
“I miss you, I tried my best to do the same things you do but I think there will be other opportunities,” she said.
The crowd clapped hoping her words ring true, with Venus then paying tribute to Muguruza.
“Congratulations Garbine, amazing,” she said.
“I know how hard you work and how much this means to you and your family. Well done today, beautiful.
“Thank you to my team who have been here day in day out, we’ve had a lot of beautiful moments in the last few weeks.”
But it was a different story in Venus’ press conference afterwards, as she gave short replies to questions from the assembled media.
When asked whether fatigue had been her downfall, or that her Sjogrens Syndrome she was diagnosed with in 2011 played a part in defeat, Williams completely avoided the question.
Venus Williams admitted she missed her sister after losing the final
“She played really well, I had a great two weeks and I’m looking forward to the rest of the summer,” she said.
“There’s always something to learn from matches you win and don’t win, but it’s always about looking forward.”
Venus added that she had not yet spoken to Serena but “she would”.
And when asked whether she would be returning to Wimbledon next year, Williams just said: “Presumably yes.”