Stormers captain Siya Kolisi will lead the Springboks against England in June, while Pieter Steph-du Toit will take the armband for Saturday's historic Test in Washington DC, against Wales.
South Africa coach Rassie Erasmus, who captained the Boks once during his playing days as flanker, also confirmed his 26-man travelling squad for the Welsh encounter in the US.
Both men will captain the Springboks for the first time, and the coach said they were deserving of the accolade: "It's a huge honour to captain the Springboks and Siya and Pieter-Steph are two honest, hardworking men who enjoy the respect of their fellow players.
"I believe both of them will do a good job as captains. My philosophy is that each player must take responsibility for his position and must therefore work extremely hard with that one goal in mind - to make the Springboks successful again."
Loose forward Kolisi is also the Stormers captain, and will be the first black player to lead the Boks in their 127-year history. He has played in 28 Tests since making his debut at age 22 against Scotland in Nelspruit on 15 June 2013. He has four Test tries to his name.
Du Toit made his debut as a 21-year-old on 9 November 2013 against Wales in Cardiff. He is equally at home as lock and as loose forward and has played in 32 Test for the Springboks - 21 as lock, 10 as flank and once as No 8.
All except two of the 43 players reported for Springbok duty on Sunday in Johannesburg, where the squad immediately got their preparations underway for this weekend's Test against Wales.
The experienced duo of Frans Steyn (centre) and Bismarck du Plessis (hooker) will join the Springbok squad next Monday following the completion of their French club rugby commitments.
Erasmus will announce his starting line-up for the Welsh match on Wednesday, just a few hours before the 26-man squad flies out to Washington.
The squad members not involved in the Welsh match will stay behind in Johannesburg to continue with their preparations for the coming international season, which starts on 9 June against England in Johannesburg.
Squad to face Wales in Washington (name, position, franchise, Test caps, points):
Forwards (16):
Nizaam Carr (loose forward, DHL Stormers, 5, 0)
Dan du Preez (loose forward, Cell C Sharks, 3, 0)
Pieter-Steph du Toit (lock, DHL Stormers, 32, 20 - 4t)
Thomas du Toit (prop, Cell C Sharks, uncapped)
Jason Jenkins (lock, Vodacom Bulls, uncapped)
Steven Kitshoff (prop, DHL Stormers, 23, 5 - 1t)
Wilco Louw (prop, DHL Stormers, 5, 0)
Frans Malherbe (prop, DHL Stormers, 17, 0)
Bongi Mbonambi (hooker, DHL Stormers, 14, 5 - 1t)
Oupa Mohojé (loose forward, Toyota Cheetahs 18, 0)
Ox Nche (prop, Toyota Cheetahs, uncapped)
Sikhumbuzo Notshe (loose forward, DHL Stormers, uncapped)
Marvin Orie (lock, Emirates Lions, uncapped)
Chiliboy Ralepelle (hooker, Cell C Sharks 23, 5 - 1t)
Kwagga Smith (loose forward, Emirates Lions, uncapped)
Akker van der Merwe (hooker, Cell C Sharks, uncapped)
Backs (10):
Curwin Bosch (utility back Cell C Sharks, 1, 0)
André Esterhuizen (centre, Cell C Sharks, uncapped)
Warrick Gelant (fullback, Vodacom Bulls, 2, 5 - 1t)
Travis Ismaiel (wing, Vodacom Bulls, uncapped)
Elton Jantjies (flyhalf, Emirates Lions, 23, 203 - 2t, 38c, 39p)
Jesse Kriel (centre, Vodacom Bulls, 29, 40 - 8t)
Makazole Mapimpi (wing, Cell C Sharks, uncapped)
Embrose Papier (scrumhalf, Vodacom Bulls, uncapped)
Ivan van Zyl (scrumhalf, Vodacom Bulls, uncapped)
Cameron Wright (scrumhalf, Cell C Sharks, uncapped)