Despite going undrafted in the NHL Entry Draft, Conklin's standout performances in both the USHL and NCAA drew attention. In 2001, he signed his first professional contract with the Edmonton Oilers, marking the beginning of his NHL career. Throughout his NHL career, Conklin played for several teams, including the Columbus Blue Jackets, Buffalo Sabres, Pittsburgh Penguins, St. Louis Blues, and two stints with the Detroit Red Wings. He made significant contributions to each team, showcasing his talent and versatility as a goaltender. Conklin's journey also included international play for the United States at the IIHF World Championship, where he earned a bronze medal in 2004. He represented his country in multiple tournaments, demonstrating his skill on the global stage.