The instalments totalled the full entitlement under his two-year contract as editor of the now defunct tabloid which was published by New International, it was claimed.
His severance package also included continued access healthcare as well as keeping hold of his company car, the corporation said.
A Labour spokesman said: “David Cameron now faces allegations that one of his top advisers was also in the pay of News International.
“The Prime Minister needs to immediately make clear whether these allegations are true.
“There are serious questions to answer about Mr Coulson’s employment in Downing Street and the country should not have to wait for full transparency.”
Mr Coulson was hired by the Conservative party in July 2007 on a reported salary of £275,000, six months after he quit as editor of the Sunday newspaper when its royal editor Clive Goodman and private investigator Glenn Mulcaire were jailed for hacking into the voicemails of Buckingham Palace staff.