Cowen was exposed to politics at a young age. His grandfather was a councillor in the Fianna Fáil party, and his father, Bernard Cowen, held a seat in the Dáil (lower house of parliament). He was an exemplary debater in school and often spoke at his father's election rallies. Cowen studied at University College, Dublin, and the Incorporated Law Society of Ireland, where he was trained as a solicitor. His father's death in 1984 prompted a by-election for the seat he had held in the Dáil. Cowen, then age 24, captured the seat, becoming one of the youngest members ever to sit in the Dáil.

Cowen's political mentor was Albert Reynolds (Reynolds, Albert), who became prime minister in 1992, at which point Fianna Fáil was in a coalition government with the Progressive Democrats. Cowen was an outspoken critic of the coalition, famously stating about the Progressive Democrats, “When in doubt, leave them out!” He served as minister of labour (1992–93), and, in 1993, after the breakup of the Fianna Fáil–Progressive Democrats government, he helped to negotiate the short-lived coalition of Fianna Fáil and the Labour Party. Cowen then served as minister for transport, energy, and communications (1993–94), leaving office after Fianna Fáil was forced into opposition by the formation of a Fine Gael–Labour– Democratic Left coalition.

During Fianna Fáil's years out of government, Cowen served successively as opposition spokesperson for agriculture, food, and forestry (1994–97) and health (1997). Following elections in 1997, Fianna Fáil leader Bertie Ahern (Ahern, Bertie) formed a coalition government with the Progressive Democrats, and the party once again returned to power. Cowen served as minister for health and children (1997–2000), foreign affairs (2000–04), and finance (2004–08). In June 2007 he was appointed deputy prime minister.

Cowen was known for his sharp tongue and sometimes rough-hewn manner, but he was also recognized for fierce intelligence, wit, and jovial demeanour among constituents. A combative politician and loyal party member, Cowen was for many years seen as an obvious successor to Ahern. In April 2008, amid an investigation into possible past financial misconduct, Ahern announced that he would resign as prime minister and leader of Fianna Fáil the following month. Cowen, who had remained supportive of Ahern throughout, was elected head of Fianna Fáil in April 2008, and he became prime minister the following month.