The 31-year-old scrum-half replaces Ruan Pienaar for the penultimate-round southern hemisphere championship match at Newlands in Cape Town.
Japan-based Pienaar last started for the green and gold against Australia in a 2011 Rugby World Cup quarter-final in Wellington.
Recalled to the squad last month. he came off the bench to score a try and help rout Argentina in Soweto, but was unavailable for the return match and an Australasia tour.
Pretoria-born Du Preez was part of the 2007 Rugby World Cup-winning South African team and has scored 70 points in 63 appearances for his country.
His return is one of two changes from the team that started in a 29-15 defeat by the New Zealand All Blacks in Auckland two weeks ago.
The other sees hooker Adriaan Strauss replace Bismarck du Plessis, who was controversially red-carded during the Eden Park Test.
Du Plessis was incorrectly sin binned during the opening half after making a hard but legal tackle on All Blacks playmaker Dan Carter.
And when the forward was justifiably yellow carded soon after half-time for leading with his elbow against Liam Messam, he was shown an automatic red card.
The International Rugby Board (IRB) and southern hemisphere body SANZAR later admitted French referee Romain Poite blundered over the first yellow card.
Springboks coach Heyneke Meyer told a media conference after the team announcement in Cape Town that the two changes had been planned.
"We were always going to rotate players where possible and planned to start this Test with Adriaan and Fourie," he said.
Meyer hailed fly-half Morne Steyn and tighthead prop Jannie du Plessis, who will win their 50th Test caps this weekend.
"They have endured through difficult times, showing a lot of resilience, and that is why they have reached this special milestone.
"It is a well deserved honour, and a privilege only a very small percentage of Springboks have achieved," added Meyer.
South Africa are seeking a 'double' over Australia this season having buried a Brisbane bogey by winning 38-12 there this month.
Title-holders New Zealand top the Championship table with 18 points after four rounds, South Africa have 14, Australia four and Argentina two.
Team (15-1)
Zane Kirchner; Willie le Roux, JJ Engelbrecht, Jean de Villiers (capt), Bryan Habana; Morne Steyn, Fourie du Preez; Duane Vermeulen, Willem Alberts, Francois Louw; Flip van der Merwe, Eben Etzebeth; Jannie du Plessis, Adriaan Strauss, Tendai Mtawarira
Replacements: Bismarck du Plessis, Gurthro Steenkamp, Coenie Oosthuizen, Juandre Kruger, Siya Kolisi, Ruan Pienaar, Patrick Lambie, Jan Serfontein
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