Hanahoe made his debut on the inter-county scene when he lined out for Dublin as a dual player in the respective minor grades. After little success, he made his senior debut in a challenge game in 1964. Over the course of the next fifteen years, Hanahoe won three All-Ireland medals, beginning with a lone triumph in 1974, followed by back-to-back triumphs as captain in 1976 and 1977. He also won six Leinster medals, two National Football League medals and one All Star. He played his last game for Dublin in September 1979.