Two run-outs of skipper AB de Villiers (16) and David Miller (1) within a space of six deliveries started the slide from which South Africa could never recover with nearly all the Indian bowlers becoming successful in choking up the runs.
Virat Kohli-led Team India, which incurred contrasting fates in the previous two encounters - a 124-run win against arch rivals Pakistan in the opening clash and a 7-wicket defeat against the islanders Sri Lanka in the second - a slip up today would result into a premature end to the defending champions' journey in England.
India have lost both the tosses in the Champions Trophy 2017 and they have had mixed results.
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Virat Kohli's side must win their last Group B fixture to avoid an embarrassing exit and they rose to the challenge after electing to bowl first at The Oval.
Indian skipper and one of the current One Day global greats, Virat Kohli doesn't have a great average against the Proteas. Probably two of the strongest teams in the tournament but only one of them will progress to the semi-finals.
Dhawan's liking for ICC tournaments began way back in the 2004 Under-19 World Cup, where he scored 505 runs with three centuries in seven innings. However, Mr 360 could only manage to score 360 before he was run out. He is also the sixth Indian to achieve the feat.
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If that run-out was unlucky, the next - which saw Miller depart for just one as both he and du Plessis ended up at the same end following a lack of communication between the pair.
That brought De Villiers to the crease as he looked to bounce back from a golden duck against Pakistan - the maiden first ball failure of his long and successful ODI career.
Kumar lined up a hat-trick ball by taking Morne Morkel for a golden duck, as he edged a simple catch to Kholi.
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It was a needless mistake indicative of South Africa's malaise and Faf du Plessis was next to perish, for 36, after failing to read Pandya's slower ball.