Veteran five-eighth after injury to first-choice Pat Lambie.
The 31-year-old was recalled from holidays after having already completed his season in France with Stade Francais in an unexpected revival of his international career.
Steyn was presumed to have played his last match for the Springboks after a making a solitary appearance at last year's World Cup in England.
But a long-term injury to Handre Pollard and Lambie being ruled out of the second test in Johannesburg on Saturday, means a route back for Steyn, who has scored 694 points in his 60 test appearances.
Lambie suffered concussion after being pole-axed by a late tackle in Saturday's 26-20 defeat in the first test at Newlands.
Steyn steps in as cover for Elton Jantjies, who will be the Boks' pivot at Ellis Park.
The third Test between South Africa and Ireland will be played in Port Elizabeth on June 25.
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