Following the abolition of the dual mandate in 2003, Humphreys was co-opted onto Monaghan County Council in succession to Seymour Crawford. She was elected in her own right at the 2004 and once again in 2009 local elections. She was elected as Mayor of Monaghan County Council in 2009. While a member of the council, she served as Chair of the council's Strategic Policy Committee on Planning and Economic Development. Humphreys was elected as a Fine Gael TD for Cavan–Monaghan at the 2011 general election. She is the only Presbyterian member of the Oireachtas. After an initial period on the backbenches, Humphreys was appointed Minister for Arts, Heritage and the Gaeltacht, following a cabinet reshuffle in July 2014. Following the formation of a Fine Gael minority government in May 2016, Humphreys was appointed to the newly created position of Minister for Arts, Heritage, Regional, Rural and Gaeltacht Affairs.
In government
Humphreys was a surprise appointment to the position of Minister for Arts, Heritage and the Gaeltacht, following a cabinet reshuffle in July 2014. After just a few months in the position she became embroiled in controversy over her appointment of John McNulty to the board of the Irish Museum of Modern Art. McNulty was a Fine Gael candidate for a Seanad by-election and his appointment occurred a few days before his nomination was announced. Humphreys was accused of stroke politics and cronyism. In her role as the Minister responsible for the preparations of the 2016 Easter Rising centenary celebrations, she said: Humphreys was appointed to the newly expanded position of Minister for Arts, Heritage, Regional, Rural and Gaeltacht Affairs following the formation of a Fine Gael minority government on 6 May 2016. On 30 November 2017, Humphreys was appointed as Minister for Business, Enterprise and Innovation. She succeeded Frances Fitzgerald, who had resigned on 28 November. On 27 June 2020, Humphreys was appointed as Minister for Social Protection and Minister for Community and Rural Development and the Islands by TaoiseachMicheál Martin.
Animal cruelty case
In February 2020, Humphreys said that she had delivered a letter to the Department of Agriculture which reportedly included "unfounded allegations" against officials prosecuting a man in her constituency with a record of convictions for cruelty to animals. An ongoing case against the man was withdrawn ahead of the scheduled trial. According to The Sunday Times, the Department of Agriculture had received the letter on 24 January and told the man's solicitor on 29 January that it would not prosecute over injured and sick animals found on his land in February 2017. In March 2020, the newspaper used records acquired under the Freedom of Information Act to report that the man's family had made "representations" to Humphreys and that a veterinary inspector participating in the prosecution asked to know who had brought the case to an end without his knowledge. In July 2020, the newspaper reported that a whistleblower had made a protected disclosure about the dropped case which showed that one official participating in the prosecution had used special legislation to tender "serious allegations" about the affair. The newspaper later reported that Humphreys's letter had included "a veiled threat" to make public information which the Department of Agriculture would prefer to keep secret.
