[4] In 1997, Cullen was appointed Minister of State at the Department of Finance by the Fianna Fáil–Progressive Democrats coalition government that came to office after the general election.

He was given responsibility for the Office of Public Works where he made huge progress in restoring the reputation of that department with number of high-profile projects, such as Leinster House 2000 and the purchase of the Farmleigh estate from Edward Guinness.

Two independent reports have cleared him of any wrongdoing in the awarding of lucrative Public Relations contracts to Monica Leech, who subsequently became President of Waterford Chambers of Commerce.

With the support of a majority of Dáil Éireann, he was the minister responsible for the stock market flotation of Aer Lingus,[5] Ireland's national airline.

Some critics at the time suggested that it was important that Ireland, as an island nation, retain control of an airline in order to ensure connectivity to nearby countries.

[6] In May 2005, Minister Cullen told Dáil Éireann that "in the context of any decision to reduce State ownership in Aer Lingus, all the options available within the regulatory framework will be examined to ensure adequate ongoing access to Heathrow for Irish consumers".

[15] The airport access slots are held by Aer Lingus for historical reasons, as the national carrier for the Republic of Ireland.

[18] In December 2008 he courted controversy by commenting on national radio that he would be supportive of having an Irish football club taking part in England's Premier League, despite the damage such a development would have on domestic football in Ireland, and the comments were also seen as unsuitable for the Minister for Arts, Sports, and Tourism.

In March 2009, a helicopter which was carrying him from Killarney to Dublin made an emergency landing shortly after take-off, because a door had fallen off.

[20] On 21 January 2010, he published his speech to the forum on Defamation Law, in which he spoke of his experiences of false allegations of adultery in the press.

He felt it had been "like waking up every morning and being raped", that he had been photographed on the front pages of Sunday newspapers for 13 consecutive weeks and that his sons had "had the living daylights"[21] beaten out of them for defending their father's honour and had to be removed from school due to "horrendous bullying".

[23] Cullen announced his resignation from his ministerial office and as a TD on 8 March 2010, due to a back ailment that had been troubling him severely in the preceding months.