Son of an American stepfather[2] and German mother, Wagner played for the United States national team, earning eight caps from 1996 until 1998.

In November 2015 took the manager's position at Huddersfield Town, whom he led to the Premier League via the 2017 EFL Championship play-off final.

In the mid-1990s, Wagner was one of several German-born players called up by United States men's national soccer team coach Steve Sampson due to their ancestry, along with Thomas Dooley and Michael Mason.

[6] Wagner made his debut in a friendly 3–1 win over El Salvador in Los Angeles on 30 August 1996, in which he was substituted at half-time for Brian McBride.

On 2 May 1997, FIFA announced that Wagner was eligible to play for the United States because his games with the German teams were exhibitions, not official matches.

[12][15] In the summer of 2016, Wagner brought in 13 players from across the continent, including Danny Ward, Chris Löwe, and Aaron Mooy.

[16] The team's success in the early 2016–17 season was largely accredited to the squad's tight bond, something that Wagner claimed was a direct result of this Sweden trip.

"[25] On 14 January 2019, Wagner and Huddersfield Town agreed to terminate his contract by mutual consent, with the team in last place and eight points from safety.

In the summer of 2021, Wagner was heavily linked with the vacant manager's position at recently relegated Championship club West Bromwich Albion, however talks broke down.

[33] Having won three qualifying rounds, the team took part in the UEFA Champions League group stage where they came last with one victory, a 2–1 home win over Manchester United in the opening fixture on 14 September.

[35] On 6 January 2023, Wagner returned to England when he was appointed head coach of Championship club Norwich City on a twelve-month rolling contract.