The Indians first bundled out Sri Lanka for 201 and then overcame some anxious moments before Dhoni (45 off 52 balls) took the team home with just two balls to spare in a dramatic title clash here.
Needing 15 from the last over in their chase of 202, Dhoni, returning to the team after recuperating from a hamstring injury, smashed Shaminda Eranga for two sixes and a boundary in just four balls to finish off the game in style at the Queen's Park Oval.
The result also meant that the Champions Trophy winners' recent run of success in the 50-over format continued.
As the captain slammed Eranga over extra cover for the winning shot, the Indian crowd erupted in joy and the jubilant players ran down the pitch to flank the man of the moment, who remained unbeaten.
Coming in at the fall of Suresh Raina's wicket with India in a spot of bother at 145 for five in the 35th over, Dhoni added important runs with the lower order and in the process hit five fours and two sixes.
Dhoni was calculative and waited till the end before launching that one final assault which left the Lankans shell-shocked as the islanders had fancied their chances after Rangana Herath's four-wicket burst on a pitch that was not conducive for strokeplay.
While Dhoni played the match-winning knock, Rohit Sharma, who hit five fours and a six, top-scored for India with 58 off 89 balls. Raina contributed 32 off 27 balls.
In pursuit of what seemed like a modest target, India lost Shikhar Dhawan and Virat Kohli early to Eranga.
Sharma found an ally in Dinesh Karthik with whom he added 50 runs for the third wicket before the wicketkeeper-batsman was dismissed for 23. Sharma then forged a 62-run stand in eight overs with Raina to consolidate India's position.