Between 1932 and 1937 Dillon served as Teachta Dála for the Donegal constituency for the National Centre Party and after its merger with Cumann na nGaedheal, for the new party of Fine Gael. Dillon played a key role in instigating the creation of Fine Gael and would become a key member of the party in later years. He remained as TD for Monaghan from 1937 to 1969. Dillon became deputy leader of Fine Gael under W. T. Cosgrave. He resigned from Fine Gael in 1942 over its stance on Irish neutrality during World War II. While Fine Gael supported the government's decision to stay out of the war, Dillon urged the government to side with the Allies. A passionate anti-Nazi, Dillon described the Nazi creed as "the devil himself with twentieth-century efficiency". His zeal against Hitler drew him the ire of the German minister to Ireland Eduard Hempel, who denounced him as a "Jew" and "German-hater". Even Eamonn De Valera, then Taoiseach, was not spared the fierceness of Dillon's rhetoric; when the Taoiseach ridiculed Dillon's stark support for the Allies, noting this meant he had to adopt a Pro-British stance, Dillon defiantly retorted Dillon had a personally eventful 1942: While holidaying in Carna, County Galway he met one Maura Phelan of Clonmel on a Friday. By that Monday the two were engaged and six weeks after that the pair were married. James was 40, Maura 22 years of age. Dillon was one of the independents who supported the first inter-party government, and was appointed Minister for Agriculture. As Minister, Dillon was responsible for huge improvements in Irish agriculture. Money was spent on land reclamation projects in the areas of less fertile land while the overall quality of Irish agricultural produce increased. Dillon rejoined Fine Gael in 1953. He became Minister for Agriculture again in the second inter-party government. In 1959 Dillon became leader of Fine Gael, succeeding Richard Mulcahy. He became president of the party in 1960. In 1965 Fine Gael lost the general election to Seán Lemass and Fianna Fáil. The non-Fianna Fáil parties won 69 seats to Fianna Fáil's 72. Had the other parties won four more seats between them, they would have been able to form a government. Having narrowly failed to become Taoiseach, Dillon stood down as Fine Gael leader after the election. On Northern Ireland, while Dillon stood against Partition, he equally opposed any "armed solution" or militant nationalist policy, stating: Dillon was a colourful contributor to Dáil proceedings and was noted for his high standard of oratory. He remained a TD until 1969, when he retired from politics. He died in Dublin in 1986 at the age of 83.