Flanker Siya Kolisi will become South Africa’s first black Test captain in the three-match series against England next month.
The 26-year-old – who has played 28 international Tests – replaces the injured Warren Whiteley as captain.
Pieter-Steph du Toit will captain the Springboks in Saturday’s match against Wales in Washington DC, USA.
“I believe both of them will do a good job as captains,” said head coach Rassie Eramus.
“It is a huge honour to captain the Springboks and Siya and Pieter-Steph are two honest, hard-working men who enjoy the respect of their fellow players.”
Chiliboy Ralepelle became the first black player to skipper the South African national team when they faced a World XV in England in 2006, but the match did not have Test status.
Rugby in South Africa has struggled to shake off the belief it is a ‘white’ sport, after black people were barred from playing during apartheid.
South African Rugby and the government have agreed that 50% of the Springboks’ team at the 2019 Rugby World Cup in Japan should be black.
England’s tour of South Africa starts on 9 June at Ellis Park in Johannesburg.