Vermeulen has been handed the No.8 jersey as one of five changes to the Springboks starting XV following the 16-16 draw with Argentina.
Juandre Kruger and Ruan Pienaar also come into the line-up, while Willem Alberts moves to the flank and Francois Hougaard switches from scrum-half to the wing.
Cheetahs fly-half Johan Goosen is also poised to make his first appearance for the Springboks after being named on the bench, with Bath flanker Francois Louw and Lwazi Mvovo also included among the replacements.
"We've decided to put Duane straight into the starting team because he is a classic No.8, a position we've lacked in since Pierre Spies got injured and Ryan Kankowski moved to Japan," said head coach Heyneke Meyer.
"I've always admired the way Duane plays rugby and he's fitted in very well the past week. He would've been a Springbok years ago if it had not been for injuries and it's great to finally see him selected.
"The same goes for Johan, who in my mind can become one of the great fly-halves in world rugby. I've been very impressed with his work ethic and attitude since he joined the squad on Thursday in Johannesburg and we will keep on managing him carefully over the next few weeks.
"Ruan brings a more tactical approach to scrum-half, while I've always been impressed with Francois at wing.
"At lock, we've decided to go for Juandre as he plays more to the ball. Juandre and Eben played well as a combination in the June Tests against England. And by including Francois on the bench, we have a specialist opensider, but also a versatile loose forward that brings a bit more balance to our back row mix."
South Africa: 15 Zane Kirchner, 14 Bryan Habana, 13 Jean de Villiers (c), 12 Frans Steyn, 11 Francois Hougaard 10 Morné Steyn, 9 Ruan Pienaar, 8 Duane Vermeulen, 7 Willem Alberts, 6 Marcell Coetzee, 5 Juandre Kruger, 4 Eben Etzebeth, 3 Jannie du Plessis, 2 Adriaan Strauss, 1 Beast Mtawarira.
Replacements: 16 Tiaan Liebenberg, 17 Pat Cilliers, 18 Flip van der Merwe, 19 Francois Louw, 20 Johan Goosen, 21 Pat Lambie, 22 Lwazi Mvovo.
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