Brought into the squad only after first-choice opener Murali Vijay was ruled out due to injured, Dhawan made full use of the opportunity and played an entertaining 168-ball innings to anchor the Indian innings.
Dhawan's blitzkrieg, combined with Cheteshwar Pujara's patient 144 unbeaten off 247 balls, powered India to their highest total on day one of an away Test and also the best by a visiting team in Sri Lanka, bettering the West Indies.
It was a case of two contrasting hundreds but both served India's purpose quite well against a home team, which was down to 10 men after middle-order batsman Asela Gunaratne was ruled out of the series with a fractured left thumb. Gunaratne was injured while fielding at second slip, trying to grab a catch of Dhawan.
The visiting batsmen were in marauding form and amassed the highest number of runs on the opening day of a Test by a visiting team in Sri Lanka.
India improved on their previous record of most runs scored on the opening day of an overseas Test, which stood at 375/9 versus New Zealand in Wellington.
But Ajinkya Rahane (39 batting, 94 balls, 1 four) put on 113 runs with Pujara for the fourth wicket and saw out the remainder of the session without any trouble.
They crossed the 50-mark off 96 balls and then the 100- mark off 182 balls. India crossed 300 in the 63rd over, and then 350 in the 77th over, with the run-rate slowing down a tad as compared to the first two sessions when Dhawan was at the crease.
Earlier, Dhawan scored his highest Test score as India reached 282/2 at tea. After lunch, Dhawan and Pujara brought up their 100-partnership off 130 balls.
The left-handed opener reached his fifth Test hundred off 110 balls, inclusive of 16 fours. He had scored at an awe- inspiring strike rate of 91.81 until then, and accelerated once he crossed this landmark. In total, he scored at 113.09 during his stay at the crease.
Shortly afterwards, Dhawan crossed his previous best score of 187 against Australia scored at Mohali in March 2013 and looked primed for scoring his maiden Test double hundred.
But it wasn't to be as he miscued a shot straight to Angelo Mathews at mid-off off Nuwan Pradeep (3-64) minutes before the tea break, and threw away his wicket needlessly.
For Sri Lanka, Danushka Gunathilaka was handed his maiden Test cap as well.
Dhawan opened the innings with Abhinav Mukund (12) and the two batsmen got off the blocks very quickly. Despite a sprinkling of green on the Galle pitch, pacers Pradeep and Lahiru Kumara (0-95) couldn't make optimal use of the new ball. The opening duo scored at will as they rotated strike with ease.
Spin was introduced in the seventh over but it wasn't stand-in skipper Rangana Herath who came on to bowl. Instead, off-break bowler Dilruwan Perera (0-103) was introduced into the attack.
He didn't make any positive impact on Dhawan, or his new partner as Pujara also made a positive start to his innings. The pair looked to attack against spin but after a few misses, settled down to form a partnership. They put on 50 runs off only 60 balls, setting the pace for the remainder of the day.
Meanwhile, Gunaratne has been ruled out from further participation in this Test series owing to a broken thumb.
Herath (0-92) finally came on to bowl in the 19th over, but the batsmen had an easy time until lunch, bringing up India's 100-mark in the 25th over.
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