The former minister had been criticised for promoting the initiative.
But the department has said she and her colleagues were only made aware of the budgetary pressures in February 2016.
They received the information in a letter from the then Department of Enterprise Minister Jonathan Bell.
Another letter from Mr Bell was received in November 2015 which contained details on proposed changes to tariffs, but did not mention the financial crisis.
Mrs O'Neill, who is now Sinn FÃ©in's Stormont leader, previously defended her role in promoting the scheme saying Sinn FÃ©in "shut it down straight away" when the issues arose.
The RHI scheme was set up in 2012, intended to increase the creation of heat from renewable sources.
However, businesses have been receiving more in subsidies than they are paying for renewable fuel and the scheme became highly oversubscribed.
A Department for Agriculture spokesperson said: "While DETI officials may have mentioned the new tariffs during presentations on RHI at some information events connected to the renewable energy training programme in the autumn of 2015, the department itself was given no indication of the budgetary pressures involved.
"On the 5th February 2016 Mr Bell wrote to First and deputy First Minister, copied to all his Ministerial colleagues, seeking agreement to take an urgent decision on the closure of the RHI scheme. It was only in this latter correspondence that Mr Bell mentioned affordability and budgetary pressures."
Michelle O'Neill only learned of the huge hole in the Renewable Heat Incentive (RHI) budget at the time the scheme was closing, the Department for Agriculture has confirmed.