Miller was raised in Woodbury, New Jersey, and played for a youth team based in Pittsgrove Township as well as Bishop Eustace Preparatory School.[4] He spent his entire college career at Northwestern University in Illinois and made a total of 77 appearances for the Wildcats. Miller finished with 36 career shutouts, setting a new school record.[citation needed] He majored in communications and minored in English while at Northwestern University and worked for MLS club Chicago Fire as an intern. Miller also trained with the team during his internship.[5]
Miller missed the rest of the USL season while recovering from thumb surgery.[13] He signed a first-team contract with the Sounders at the end of the year.[13] While initially expected to be a bench player, Miller made his first-team debut in the second match of the 2016 season after starter Stefan Frei was ruled out with an injury. The team lost 2–1 to Real Salt Lake during the match, which was played on Miller's birthday.[14] His next match for the Sounders was a 2016 U.S. Open Cup match, also against Real Salt Lake, in which Miller made several saves to win a penalty shootout.[15] He played in two more U.S. Open Cup matches and was on the bench during the team's MLS Cup 2016 victory; Miller also played in several USL matches for Seattle Sounders FC 2.[16] He made one regular season appearance in 2017 but was later called up for a MLS Cup Playoff match against the Houston Dynamo, where Miller kept a clean sheet.[17]
Los Angeles FC
On December 12, 2017, Miller was selected by Los Angeles FC with the first selection in the 2017 MLS Expansion Draft.[18] On March 4, 2018, Miller debuted in a match against his former team, the Seattle Sounders. He made seven saves to keep a clean sheet as LAFC won 1–0.[19]
Miller went on to play in 33 matches for LAFC in their inaugural season, as Luis López was injured at the start of the year. He earned 10 shutouts in the regular season.[20]
Minnesota United
On January 16, 2020, Los Angeles FC traded Miller to Minnesota United FC in exchange for $150,000 GAM in 2020 and $50,000 TAM in 2021. The transaction included Minnesota signing Miller to a new contract through the 2022 season with a club option for an additional year.[21] On August 19, 2020, the club announced that Miller had undergone hip surgery and would miss the remainder of the 2020 season.[22] He later returned to the club as a starter for the 2021 season, but was later replaced in 2022 by Dayne St. Clair.[5]
D.C. United
On November 23, 2022, Miller signed with D.C. United as a free agent ahead of their 2023 season.[23] He became their starting goalkeeper and was assigned to play as a sweeper-keeper by manager Wayne Rooney.[24][25] Miller was selected by Rooney to play in the 2023 MLS All-Star Game against Arsenal F.C., which was hosted by D.C. United.[26] In August, Miller suffered a torn rotator cuff and underwent season-ending shoulder surgery.[27] D.C. United declined his contract option following their 2024 season.[28]