India thus lead the five-match series 2-1.
Kohli's 134-ball knock was ably complemented by an under-pressure skipper Dhoni (80 off 91) as the duo forged a 151-run partnership off 163 balls to effectively seal the match with 10 balls to spare after the home team made a shaky start in their pursuit of 286.
Dhoni for one promoted himself up the order after much deliberation and it did yield results.
Eventually, it was India's No 1 batsman Kohli, who got the job done with ridiculous ease. He is amassing hundreds at a staggering rate and today was his 26th one in ODIs. He has now scored three hundreds in his last seven ODI innings and has a batting average of 52 plus in 174 matches. He hit 16 boundaries and a six.
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India's batting mainstay also had luck on side as he was dropped on 6 by Ross Taylor, who could not hold to a regulation catch standing at a wide slip on the bowling off Henry.
On the way to his first half century in 11 innings, Dhoni completed 9000 runs to become the fifth Indian to do so after Sachin Tendulkar, Sourav Ganguly, Rahul Dravid and Mohammad Azharuddin. He also surpassed Tendulkar to be India's leading six-hitter in ODIs.
At a packed PCA stadium, the dew also played its part in the evening keeping the grounds men busy during drinks break. India felt the pressure at the start of the chase. Openers Rohit Sharma and Ajinkya Rahane, who were not among the runs in the earlier games, fell cheaply once again.
While Kohli looked in sublime touch at the other end, Dhoni promoted himself at number four ahead of Manish Pandey in his bid to lead from the front in a tricky situation.
(REOPENS DEL 32)
The visitors were let down by the senior batsmen in the team including captain Smith, who pottered around for 95 balls to make 27 before having a rush of blood, falling to Ashwin who also got the wicket of Renshaw later.
The Indian spin bowlers were shuffled around by captain Virat Kohli, which never allowed the batsmen to settle down.
The trio of Indian spinners had Australia on the hop by striking three blows after lunch they could not recover till Starc's counter-punching knock as hit a six each off Ashwin, Jadeja and Ishant Sharma.
There was turn for the Indian spinners but the track was not the cause of the Australian batsmen's downfall as they lost their way after a sound start by Warner, who played an unusually subdued innings of 38 in 77 balls with six fours, and Renshaw.
After tea, Jadeja packed off Mitchell Marsh (4) by trapping the batsman plumb in-front and then Umesh struck again to have Wade leg before that left the visitors at a difficult 190 for six as Renshaw held one end up with diligent batting.
Ashwin then struck an important blow by having the stubborn Renshaw caught at second slip. The lanky batsman prodded at one that turned away across the bat and the edge was taken by Murali Vijay.
Smith continued his defensive ways after lunch but a
double blow saw the visitors' captain and Peter Handscomb depart late in the second session.
Handscomb was caught right in front of the wicket by Jadeja with a quicker, straight ball and five balls later Ashwin had Smith caught at mid-wicket coming down the track in a rush of blood.
Handscomb batted for 45 balls while Smith faced 95 balls and struck just two fours.
And when Renshaw was dismissed by Ashwin, the end of the innings was in sight with Australia at 196 for 7, having all seven wickets in less than 50 overs and for the addition of 114 runs.
Renshaw, playing in only his fifth Test, the other Australian top line batsmen did not know how much to attack and how well to defend.