Dhoni smashed a 38-ball 58 after Gambhir (88 off 99 balls; 7x4) and Tiwary 65 off 68; 6x4) put India on course with a 110-run partnership for the fourth wicket at the Pallekele International Cricket Stadium.
Dhoni along with Irfan Pathan (29 not out) plundered 77 runs in just 9.5 overs before falling to Lasith Malinga in the penultimate over of the innings.
Dhoni, who came to the crease at the dismissal of Gambhir, was ruthless against the Lankan bowlers, hitting them all across the park, while bringing up his 50 off just 34 balls with a huge six over midwicket off Thisara Perara.
With his three wickets, Malinga was the pick off the bowlers for the hosts, who had rested captain Mahela Jayawardene and Rangana Herath.
Opting to bat, Indian openers in the absence of rested Virender Sehwag, started off sedately with the first boundary of the innings coming in the fourth over -- Ajinkya Rahane driving Thisara Parera through the covers.
Rahene's joy was, however, shortlived as the Mumbai batsman, who was playing in his first match of the series, fell for just nine runs to an incoming delivery from Parera.
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Gambhir along with in-form Virat Kohli (23) combined together to add 48 runs for the second wicket before Nuwan Pradeep brought one in to the right-hander to have him trapped in front.
Rohit Sharma's misery with the bat continued as he became Pradeep's next victim -- the ball angling in and moving out after pitching to take the off stump of the Mumbaikar, who was looking to play towards the leg side.