Dempsey spent the majority of his 9-year tenure playing defense with the Leafs with their AHL affiliate, the St. John's Maple Leafs where he was team captain for many of his years. His most successful season came in the 2001-02 season where he scored 61 points in 75 games for St. John's. Dempsey had only played 48 games for Toronto when he left as a free agent on July 12, 2002, signing with the Chicago Blackhawks.
Nathan established himself as a NHL regular in the Blackhawks blueline in the 2003-04 season and on March 2, 2004, he was traded from the Blackhawks to the Los Angeles Kings. Dempsey spent the 2004 NHL lockout with German team Berlin Polar Bears of the DEL, before returning to the Kings for the 2005-06 season. Dempsey joined his fourth NHL team on August 7, 2006, when he signed with the Boston Bruins.