Born[1] in Phoenix, Arizona, Conklin grew up in Anchorage, Alaska, and was an early recruit of the now-famed Minnesota hockey prep school Shattuck-St. Mary's.

Subsequently, he went on to earn numerous goaltending awards and accolades in both the USHL and NCAA, however Conklin claims he never thought of becoming a professional until his junior year (his second playing) at University of New Hampshire.

[3] Before making his professional debut, Conklin spent two seasons playing for the Green Bay Gamblers of the United States Hockey League, followed by three seasons playing hockey with the University of New Hampshire's team, the Wildcats (before Conklin could join the Wildcats, he was forced to take a year off because NCAA regulations dictated he do so due to a Division I program transfer).

[4] With the completion of his career at the University of New Hampshire in the spring of 2001, Conklin signed a professional contract as an undrafted free agent with the Edmonton Oilers.

However, the extraordinarily bad timing and subsequent massive public focus on the indelible miscue did nothing to improve his reputation, already severely diminished by a poor regular season.

He was expected to compete for the Blue Jackets' backup goaltending position, however head coach Gerard Gallant opted to go with internationally experienced Fredrik Norrena.

On July 19, 2007, Conklin was signed as a UFA by the Pittsburgh Penguins to a $500,000, one-year, two-way contract (that would pay him $100,000 in the AHL, exempting him from re-entry waivers).

[13] After being assigned to Wilkes-Barre/Scranton of the AHL on September 22, he was recalled by Pittsburgh on an emergency basis on December 6, when starting goaltender Marc-André Fleury suffered a high ankle sprain.

Before Fleury's return as a starter on March 2, 2008, Conklin compiled a record of 17–6–5, earning the nickname "Conkblock" (derived by keeping a person away from a goal, or preventing someone from scoring) by posting career numbers (such as a 50-save win over the New York Islanders at Nassau Coliseum on February 26, despite being outshot 52–21)[14] and leading the NHL in save percentage.

Due to the existence of the salary cap, the fact Pittsburgh had both Fleury and Sabourin under one-way contracts for 2008–09, and the likelihood of his ability to earn a major increase in both playing time and salary (the 50% raise that eventually came from the Red Wings, who guaranteed him 30 games, was seen as a bargain) with his 2007–08 performance, despite Conklin's significant and memorable contribution to the team, the Penguins did not renew his contract, and decided to allow him to reach unrestricted free agency once more on July 1.

[18] Along with Conklin, former Penguin Marián Hossa also signed a one-year contract with Detroit, joining the team that had just defeated them in the Stanley Cup Finals less than a month earlier.

[19] Detroit head coach Mike Babcock expressed a desire to play Conklin in every third game in order to relieve starter Chris Osgood.

[20][21] On November 17, 2008, Conklin made his debut at Detroit's Joe Louis Arena against the Edmonton Oilers, posting his fifth career shutout as the Red Wings won 4–0.

Conklin received his second taste of NHL playoff experience in Game 4 of the Western Conference Finals against the Chicago Blackhawks, where he substituted for a dehydrated Osgood in the third period and played 20 scoreless minutes.

It was announced in the 2009 off-season Conklin would not be offered a new contract for the 2009–10 season due to salary cap constraints, with the Wings instead opting to promote longtime prospect Jimmy Howard from the AHL.

[23] On July 1, 2009, Conklin signed a two-year deal worth an average of US$1.3 million per year with the St. Louis Blues, who made him an immediate offer following the start of free agency at noon.

"[24] Conklin made his debut with the Blues overseas, on October 3, facing his former team, the Red Wings, at Sweden's Globe Arena, in the second game of the doubleheader of NHL Premiere 2009 Stockholm.

Following an upset of the host Czechs and a shutout, 1–0 shootout victory over Slovakia in the bronze medal game, Conklin was selected as the tournament's best goaltender.

Following the 2011 season, Conklin returned to play for the United States at the 2011 IIHF World Championship in Slovakia, with his best performance coming on May 6 against Canada in a 4–3 shootout loss in the qualifying round.

His younger brother Brice used him for shooting practice in their basement (a reversal of the usual positions for siblings) and went on to play defense for Shattuck and for Harvard University.