Collins played collegiate tennis at the University of Virginia and won the NCAA singles title twice, during her sophomore and senior years in 2014 and 2016.

[4] She trained at the Isla Del Sol Yacht & Country Club in St. Petersburg for six years and IMG Academy from 2010 to 2012.

[4][7] She finished her college career in 2016 as the nation's top-ranked player and received the Honda Sports Award for tennis.

[9] She returned to the University of Florida for graduate school to earn a master's degree in sports management in a program partnering with the WTA.

Collins made her WTA Tour main-draw debut as a wildcard player at the 2014 US Open in the Arthur Ashe Stadium, where she forced second seed Simona Halep to a third-setter in the first round.

Collins started the year reaching the final round of qualifying at the Australian Open, before being outclassed by Denisa Allertová, in two sets.

However, she received a wildcard at the WTA 125 tournament at Newport Beach and claimed the title there, which saw her rise to a career-high ranking of No.

In the round of 16, Collins pulled off the biggest upset of the tournament, dominating the second seed and three-time major champion Angelique Kerber, in straight sets.

She achieved her best-ever Grand Slam doubles result at Wimbledon, reaching the quarterfinals with Bethanie Mattek-Sands.

In December, she won the Hawaii Open, an exhibition tournament, upon the withdrawal of her finals opponent Angelique Kerber.

[20] She lost in the second round to Yulia Putintseva at the Australian Open, and dropped outside the top 50 due to failing to defend her semifinalist points.

Due to the six-month shutdown of the WTA Tour caused by the COVID-19 pandemic, Collins did not play again after the Australian Open until August.

1, Garbiñe Muguruza, in the third round (handing the Spaniard her earliest exit from Roland Garros since 2013) as well as 30th seed Ons Jabeur, both in three sets.

[19] Collins won her first WTA Tour title at the Palermo Ladies Open, defeating Elena-Gabriela Ruse, in straight sets in the final.

[22] The following month, she won her second WTA title at the Silicon Valley Classic, defeating Daria Kasatkina in three sets.

[27][28] In her next two tournaments, Collins reached the quarterfinals in Chicago and the third round in Indian Wells before concluding her season in Linz, where she was forced to retire in her semifinal match against compatriot Alison Riske due to a shoulder injury.

At the Australian Open, Collins reached the semifinals for the second time, after defeating 19th seed Elise Mertens to become the third American woman in the quarterfinals.

[30] She defeated Iga Świątek also in straight sets in the semifinals to advance to her first Grand Slam final, where she faced world No.

1 Iga Świątek at the 2024 Australian Open, Collins announced that 2024 would be her last year of playing professional tennis.

[63][64] The following week, she also qualified for the WTA 1000 Qatar Ladies Open and reached the quarterfinals, defeating 13th seed Veronika Kudermetova, and Czechs Marie Bouzková and Kateřina Siniaková.

[65] In Indian Wells, Collins defeated Russian qualifier Erika Andreeva and then lost to Iga Świątek in the second round.

She reached her second career WTA 1000 semifinal (after 2018 Miami) with a straight-set win against Caroline Garcia, increasing the head-to-head to 4–0.

[67][68] She secured her inaugural WTA 1000 title with a decisive victory in straight sets over Elena Rybakina, the fourth seed and previous year's runner-up.

[69][70][71] Unseeded again at the Charleston Open, she defeated Paula Badosa, and second seed and defending champion Ons Jabeur.

7 and third seed, Maria Sakkari, all in straight sets, to reach the final, extending her record to 12 consecutive match wins.

[75][76] In Madrid, Collins continued her winning streak to 15 matches, securing victories over qualifiers Olga Danilović and Jaqueline Cristian.

[83] At the WTA 500 in Strasbourg, she advanced to her third final of the season, defeating Kateřina Siniaková, Clara Burel, and Anhelina Kalinina.

[91] Collins reached the quarterfinals at the Paris Olympics but retired due to injury while trailing in the third set of her match with world number one Iga Świątek.

[97][98] Collins played her first season with World TeamTennis in 2019 with Billie Jean King's Philadelphia Freedoms.

She started the 2020 season on the Orlando Storm roster which began July 12,[99] but was dismissed from the league after leaving the state and breaching COVID-19 safety protocols.