Jayawardene made his Test debut in the record breaking Test in 1997 against India at R.P.S., Colombo. Jayawardene added 66 to their first innings score of 952/6, the highest ever Test score. He was at the crease when they surpassed the previous highest Test score. Early in his career he scored 167 against New Zealand and 242 against India.

Jayawardene's One Day International debut was against Zimbabwe at Premadasa in January 1998. They won the match, with Jayawardene hitting the winning run. In the next game Jayawardene scored a 74. It took only 11 matches before he scored his first century, which was against England in the Carlton and United World Series game at Adelaide. Jayawardene entered a pressure situation, with Sri Lanka struggling at 134/4, but made an innings of 120 runs to win the match.

Jayawardene was captain during the England tour in 2006 in the absence of Marvan Atapattu. He led his team to 1-1 draw in the Test series and an emphatic whitewash (5-0) in the ODI series.