Opposition concerns over the claims surrounding Mr Brennan shifted to Aer Rianta's role in the controversy after the Taoiseach confirmed the Minster for Transport as the Cabinet member at the centre of the allegation.
As political leaders questioned Mr Ahern about the nature of the investigation, Sinn Féin's Mr Caoimhghín Ó Caoláin and Labour leader Mr Pat Rabbitte suggested internal politics may have inspired the charge against Mr Brennan.
Mr Ó Caoláin said there was "undoubted public concern" about power relations within the airports operator, and in particular the role and performance of its chairman Mr Noel O'Hanlon. "We are concerned that Aer Rianta is seen as almost a political extension of the Fianna Fail fifedom," he said.
He said this week's revelations could be the "tip of the iceberg" and suggested a "culture of corruption" may exist at the company.
He questioned whether it was appropriate that Aer Rianta should be conducting an internal investigation and called on the Taoiseach to "initiate a proper and full inquiry into the conduct and affairs of Aer Rianta".
The Taoiseach rejected the idea.
Mr Rabbitte also expressed concern about the validity of the internal inquiries being made by Aer Rianta and the Department of Transport.
He said the suggestion that the Department, rather than the Minister, may be responsible for the alleged unpaid bill called into question whether the Secretary General should be investigating.
Fine Gael leader Mr Enda Kenny said the controversy "cast a cloud over the Government" and also questioned the wisdom of the two internal investigations.