De Villiers bruised his ribs during the Test match against Scotland last month and has not been available since.
His return is seen as a massive boost for the ailing backline, which has failed to spark during the Tri-Nations campaign thus far.
Springboks coach Jake White also added uncapped Sharks scrumhalf Ruan Pienaar and tighthead prop BJ Botha, who were both selected for his pre-season training camp but then discarded before the Tests began.
Both choices will be popular in the Republic, where criticism has been heavy following three Tri-Nations defeats so far, but despite a strong claim for selection, Stormers and Western Province flanker Luke Watson was once again ignored.
Fit-again lock Danie Rossouw returns alongside flyhalf Andre Pretorius, with the latter claiming the second spot behind Butch James.
This means that Jaco van der Westhuyzen and Meyer Bosman have both been dropped from the squad.
Van der Westhuyzen played in the 49-0 defeat to Australia and was partly blamed for the Springbok woes that day, while Bosman has not started since his poor showing on the European tour last November.
The Boks face New Zealand in Pretoria on August 26 and again in Rustenburg on September 2. They finish off the competition against Australia at Ellis Park in Johannesburg on September 9.
Australia have last won in South Africa in 2000 while New Zealand have not won a Test in the Republic since 2003.
Squad - Backs: Jean de Villiers, Fourie du Preez, Jaque Fourie, Bryan Habana, Butch James, Ricky Januarie, JP Pietersen, Percy Montgomery, Akona Ndungane, Wynand Olivier, Ruan Pienaar, Andre Pretorius.
Forwards: John Smit (capt), Eddie Andrews, Brendon Botha, Jacques Cronje, Os du Randt, Victor Matfield, Johan Muller, Chiliboy Ralepelle, Danie Rossouw, Lawrence Sephaka, Juan Smith, Pierre Spies, Solly Tyibilika, Albert van den Berg, CJ van der Linde, Joe van Niekerk.