Handley was born in Meadow Lake, Saskatchewan. Prior to moving to the NWT in 1985, he had worked as an educator. He served in a wide number of cabinet portfolios in the NWT government, including Deputy Minister of Education, Deputy Minister for the Departments of Renewable Resources, the NWT Housing Corporation, Transportation and Resources, Wildlife, and Economic Development.
He was elected to the territorial legislature in the riding of Weledeh in 1999, and subsequently served as Minister of Finance, Chairman of the Financial Management Board, Minister Responsible for the Workers Compensation Board, Minister of Transportation, and Minister Responsible for the NWT Power Corporation.
After running unopposed in the Northwest Territories general election, 2003, he also ran unopposed for premier among his colleagues in the Legislature, and was acclaimed to that position on December 10, 2003.