After a jittery opening set, Spanish fourth seed Muguruza rallied but 13th-seeded Frenchwoman Mladenovic perfectly played the key points in the decider to set up a meeting with Timea Bascinszky.
Mladenovic, who has been hampered by back problems, tops the tally of double faults produced at Roland Garros, having served 40 since the tournament started. Even though she won on Sunday, she kept adding to that total.
'Kiki, Kiki!" yelled the crowd as Mladenovic, who is of Serbian heritage, speaks good English and cheers herself up in Italian, negotiated her way through the tricky fourth-round match.
"I love you, too," she told the chanting crowd after the win on a sunbathed Court Suzanne Lenglen.
She paused.
"You make me cry," she continued. "Let me try to speak. It's a last-16 match against the defending champion. Big match, which I was waiting for.
"It's not perfect, there are little problems but I fight as I can. I served 35 doubles but it's good because you give me so much strength," added Mladenovic, who has been tipped as one of the tournament favourites after reaching the finals in Stuttgart and Madrid on clay this season.
With Alize Cornet taking on Caroline Garcia in the fourth round on Monday, two Frenchwomen will be in the last eight for the first time since 1994.
That year, Mary Pierce reached the final, losing to Spaniard Arantxa Sanchez-Vicario. Pierce went on to lift the Suzanne Lenglen Cup in 2000, the last Frenchwoman to do so.
The absence of Serena Williams, who is expecting a child, and Maria Sharapova, who was denied a wildcard on her return from a doping ban, means the draw is wide open for Mladenovic to finally end the wait for a home champion.
The 24-year-old got off to a flying start against Muguruza, who peppered the court with unforced errors as the Frenchwoman opened a 4-1 lead.
Mixing her powerful game with sliced backhands to slow down Muguruza, Mladenovic was in the driving seat after pocketing the first set.
Yet, the Spaniard was not conceding defeat and played tighter in the second set with Mladenovic looking increasingly shaky on serve.
But Muguruza was also nervous.
"I was a bit nervous and I got more and more nervous," she said. I could not find my game but I did not do anything wrong. It came from her, she was playing well."
Mladenovic opened a 2-0 lead in the decider and held serve throughout, despite three double faults in a single game.
Muguruza dinked a forehand into the net on the first match point after just under two hours.
(Editing by Clare Fallon and Pritha Sarkar)
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