John Richardson practiced law in Portland for seventeen years and developed extensive expertise in representing personal injury clients, public and private unions, and small businesses, while being in the forefront of many cases involving employment discrimination.

In 1998, John was elected to the Maine House of Representatives from Brunswick where he served as House Majority Leader from 2002-2004 and Speaker of the House from 2004-2006. While in the legislature, John sponsored the legislation which created the Mid Coast Regional Redevelopment Authority (MRRA) and served on its planning and implementing committees. In January 2007, he was appointed Commissioner of the Maine Department of Economic and Community Development, a position that he held until November 2009. As Commissioner, he served as a board member on the Finance Authority of Maine (FAME).