Hamilton played college soccer for the Denver Pioneers in her home state of Colorado, where she set multiple program records.

In the NWSL off-season in 2019–20, she played for the Western Sydney Wanderers of the W-League in Australia and received the Julie Dolan Medal as the league's best player.

She attended Columbine High School from 2006 to 2010,[5] where she was a varsity soccer player from her freshman year and committed to the University of Denver as a sophomore.

In 2012 the USL W-League was the highest tier of professional women's soccer in the US and Hamilton enjoyed a great season scoring 6 times in 10 games against some of the best players in the country.

[4][10] Hamilton was part of the Flash team that won the 2016 NWSL Championship, entering the match as a substitute in extra time.

Hamilton appeared in the semi-final game as a second-half substitute as North Carolina defeated the Chicago Red Stars to advance to their second straight final.

[4][16] While several Courage players participated in the 2019 FIFA Women's World Cup during June and July, Hamilton scored her first career NWSL hat-trick against Orlando Pride in June, followed by a four-goal match against Houston Dash in July that tied the league record for most goals scored by a player in a single match.

[4] North Carolina Courage loaned Hamilton to Western Sydney Wanderers of the Australian W-League following the 2019 NWSL season.

Her seven-goal performance tied her for the W-League Golden Boot and earned her the season's Julie Dolan Medal as the league's top player as selected by a panel of voters.

[4][22][23] On July 22, 2021, the Courage announced that it had traded Hamilton, defender Hailie Mace, and goalkeeper Katelyn Rowland to Kansas City NWSL in exchange for Amy Rodriguez.

[27] On August 25, 2021, Hamilton made her 100th NWSL appearance against Racing Louisville FC, where she scored the match-winning goal in the 40th minute.

Hamilton was the top scorer in the 2023 NWSL Challenge Cup, scoring 5 goals en route to winning the overall MVP of the tournament.

[32][33] On March 16, 2024, Hamilton came off the bench to notch a goal in the 64th minute for the Kansas City Current, who edged out the Portland Thorns 5-4 in the inaugural match at CPKC Stadium.

[36][37] On September 3, 2019, Hamilton earned her first cap with the United States senior team, coming on in the second half for fellow Courage teammate Jessica McDonald in a friendly against Portugal.