In the 1993 election, Duncan was elected as a member of the Reform Party. He has served in all that party's incarnations up until the 2006 federal election, when he lost his seat to Catherine J. Bell of the New Democratic Party by 630 votes. Duncan was the Conservative Party's Official Opposition Critic for Natural Resources. During that time he served on the Natural Resources Committee. He helped shape Conservative Party policy on west coast offshore oil and gas, softwood lumber trade and the pine beetle epidemic. While in parliament, he was a member of the "Restaurant Caucus" in the House of Commons, a group of MPs who have interests in the restaurant industry. Duncan's Private Member's Bill C - 259 passed the 38th Parliament to receive Royal Assent to eliminate the excise tax on jewelry. Duncan made parliamentary history as the first MP to have a Private Member's bill related to cutting taxation pass. He won the Vancouver Island North Conservative Party nomination for the 2008 federal election and was elected with 45.78% of the vote. On December 2, 2008, the New Democratic Party asked the RCMP to investigate John Duncan's alleged secret recording of a private NDP conference. He had apparently received the invitation to participate by mistake, in place of NDP MP Linda Duncan who had "a similar email address". This happened within the context of the 2008–09 Canadian parliamentary dispute. On August 6, 2010, in a minor cabinet shuffle, he joined cabinet as Minister of Aboriginal Affairs and Northern Development. Under the Harper government, several key bills with a direct effect on aboriginal communities have stalled. As a result, First Nations across Canada have embarked on a widespread and prolonged series of demonstrations under the banner of "Idle No More." In addition, Attawapiskat chief Theresa Spence began a fast in December 2012 to demand a meeting with Harper and a Crown representative. In response, Duncan wrote to Spence requesting she give up her hunger strike and meet with him. "I didn’t ask for Minister Duncan," Spence replied. "And I have dealt with him before. When I observe him, he doesn't have a mind of his own because, before he would answer a question, he would always look at his people. He's not the Prime Minister." On February 15, 2013, he resigned from his cabinet position as Minister of Aboriginal Affairs and Northern Development after improperly advocating to a tax court on behalf of a constituent in June 2011, and was replaced by James Moore. He returned to cabinet in the more junior role as Minister of State and Chief Government Whip in July 2013. In the 2015 Canadian federal election, Duncan sought reelection in the newly created riding of Courtenay—Alberni, but was defeated by Gord Johns of the NDP.