Electing to bat, Dhoni bailed India out of trouble with his 86-ball knock to take the team to 247 for nine. His bowlers then ended the visiting side's innings at 225 to record their first win on South Africa's current tour.
Going through the toughest phase of his international career, Dhoni played a captain's knock and then made smart bowling changes to bundle out South Africa in 43.4 overs.
Axar Patel (3/39) and Bhuvneshwar Kumar (3/41) shared six wickets between them, while Harbhajan Singh (2/51) scalped two in his comeback match.
The nudges, quick singles, shot-arm jabs, pulls, cuts, lofted shots over the bowlers' heads - all were on full display as Dhoni answered his critics with a knock that was decorated with seven boundaries and four sixes.
'Captain Cool' batted with the tail-enders with a calm head as India scored 82 runs off the last 10 overs to put on board a decent total, which at one stage looked impossible.
India were looking down the barrel at 165 for seven in the 40th over, but Dhoni found great support from Harbhajan Singh (22), with whom he added 56 runs.
Ajinkya Rahane yet again batted well, scoring a 63-ball 51 for his second consecutive half century.
For South Africa, Dale Steyn (3/49) picked up three wickets, while Morne Morkel and Imran Tahir scalped two apiece.
South Africa started their chase on a quick note, stitching a run-a-ball 40-run partnership for the opening wicket between Hashim Amla (17) and Quinton de Kock (34).
De Kock was the aggressor of the two but was lucky as a diving Rohit Sharma spilled a tough chance off Umesh Yadav in the fourth over.
With both his frontline pacer proving ineffective, Dhoni introduced spin from both ends in the sixth over. The move yielded instant result when Axar had Amla stumped after the batsman danced down the wicket.
De Kock was going great guns with five boundaries when he fell for one too many, caught by Mohit Sharma at long-off off Harbhajan, leaving the Proteas at 52 for two inside the 10th over.
The fall of two quick wickets hardly bothered Faf du Plessis (51) and JP Duminy (36) as the duo batted with ease to keep the asking rate in control.
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