[4] Naeher played the 2006 USL W-League season with the Western Mass Lady Pioneers, making 11 appearances and only allowing a 0.59 goals against average.
[8] The Breakers finished second in the WPS standings that season but lost the Super Semifinal to the Philadelphia Independence.
[11] In May 2013, Naeher signed with the Boston Breakers in the newly formed National Women's Soccer League, returning to the United States after playing for two years in Germany.
On November 22, 2015, Naeher was traded from the Boston Breakers to the Chicago Red Stars for defender Whitney Engen.
[13] Naeher had a strong start to the 2016 NWSL season in Chicago; she was named Player of the Month for May, posting three shutouts and allowing just one goal in four games.
[18] On March 23, 2024, Naeher made NWSL history by becoming the first goalkeeper with 50 wins for a single club when the Red Stars defeated Seattle Reign FC in a 2–1 victory.
[21] On December 18, 2014, Naeher made her first appearance and start for the United States Women's National Team in a 7–0 win over Argentina in the International Tournament of Brazil.
Since the United States' loss at the 2016 Summer Olympics, Naeher has become the USWNT's number one goalkeeper, taking over the spot that had been held by Solo for years.
[23] Naeher was the primary goalkeeper for the United States at the 2018 CONCACAF Championship; she played in four of the five matches and earned four shutouts.
[25] When Naeher started the team's first group game on June 11, it was the first time in over two decades that neither Hope Solo nor Briana Scurry was in goal for the U.S at a World Cup.
In the knockout round, Naeher made four saves against France in the quarterfinals to help the team preserve a 2–1 victory over the host nation.
[27] In the semifinals, Naeher had three saves and stopped Steph Houghton's penalty kick in the 83rd minute to help the United States to a 2–1 victory over England.
[28] In Sunday's final, Naeher posted one save to culminate in a shutout over the Netherlands in a 2–0 victory for the U.S., resulting in the team repeating as World Cup champions.
[36] Naeher was named the best goalkeeper of the tournament and earned the Golden Glove award for her performances as the U.S. went on to win the inaugural Gold Cup, defeating Brazil 1–0.
[39] She made key saves against Brazil's Gabi Portilho and Adriana in the final, which the United States won 1–0 on a goal from Mallory Swanson.