Will step down after upcoming Test series against Pakistan
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The middle-order batsman, who led Sri Lanka for the first time in April 2004, did not play in Tuesday's Twenty20 international here, which India won by three wickets.
"After much thought, I have concluded that the right time has now come for fresh leadership to takeover," said Jayawardene.
"It was not an easy decision to make because being the Sri Lanka captain has been the source of enormous pride. I am very grateful to have been granted the honour of leading the team."
Jayawardene however made it clear he was not quitting the team altogether.
"I look forward now to extending my full support to my successor and hope to play a major part in the team's success during coming years as a batsman," he added.
Sri Lanka Cricket chief executive Duleep Mendis said Jayawardene's resignation had been accepted, but no decision would be made on a new captain until the tour of Pakistan ends.
Jayawardene guided Sri Lanka to the World Cup final in the West Indies in 2007, where they lost to Australia.
He captained Sri Lanka in 26 Tests, winning 15, losing seven with four draws.
In 94 one-day internationals under him, Sri Lanka won 54 and lost 35 while the rest ended in no-results.
The first Test in Pakistan will be played in Karachi from February 21-25, while the second and final match will be played in Lahore from March 1-5.
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