Zirnkilton, a Republican, served for eight years (four terms) in the Maine House of Representatives from 1982 to 1988 and again from 1992 to 1994. He represented part of Hancock County, Maine, including his residence in the village of Seal Harbor in the town Mount Desert. During his final term in the House of Representatives, Zirnkilton served in leadership as Assistant Minority Leader. In 1994, when then Congresswoman Olympia Snowe decided not to seek re-election to the U.S. House of Representatives for Maine's 2nd congressional district, Zirnkilton sought to replace her. Zirnkilton lost the primary to fellow State Representative Richard A. Bennett, who eventually lost the general election to State Senator John Baldacci.