Singh's team reset the @PMOIndia account and renamed it @PMOIndiaArchive, angering the incoming Modi-led Bharatiya Janata Party (BJP) government which complained that it would have to start from scratch to build up followers.
The BJP called the action "disgraceful, unethical and illegal", adding that the PMO account was a national digital asset and not a personal one.
But Singh's office said late Wednesday that both the official account and its existing followers would be handed to Modi's government.
"The Twitter account @PMOIndia has been secured by Twitter and they are assisting in the handover of the same to this office to be available to the incoming PMO administration along with its (existing) followers," Singh's office said in a statement late Wednesday.
A restored @PMOIndia account on Twitter showed 16,023 followers on Wednesday.
Modi, who is extremely active on Twitter, has been sharing the milestones in his election campaign journey with his 4.2 million followers.
He is set to be sworn in as India's 14th Prime Minister next Monday after the BJP swept to power with the first parliamentary majority in 30 years at the end of a marathon general election.
The Congress party suffered its worst defeat ever, snaring just 44 seats out of 543 up for grabs against BJP's 282.