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Stony Brook began play in the 1969–70 season at the Division III level. The program advanced to Division II beginning in the 1995–96 year, and fully transitioned to Division I in 1999, hiring Trish Roberts as head coach.

Stony Brook played two independent seasons as before joining the America East Conference in 2001. In Stony Brook's first America East season, the Seawolves finished in seventh place but earned two upsets in the tournament to advance to the finals. Stony Brook almost reached the NCAA Tournament but fell to Hartford 50–47. Roberts failed to reach double-digit victories in her next two seasons and resigned on August 25, 2004. She cited family issues but Newsday reported that several players left the team and Roberts clashed with first team All-Conference player Sherry Jordan.

Sacramento Monarchs assistant Maura McHugh was named interim head coach on September 10 and promoted to full-time head coach on April 26, 2005 after an 8–20 season. In McHugh's second season, Stony Brook won 20 games for the first time in program history and finished a program-best second place in the regular season. On December 2, 2005, Stony Brook played No. 19 Temple, its first ranked opponent in program history, and pulled the 58–56 upset. The Seawolves lost in the conference semifinals but qualified for the WNIT, where they lost to Hofstra in the program's first-ever postseason appearance. After another second-place finish in the conference regular season in 2006–07 at 14–2, the Seawolves were upset by UMBC in the quarterfinals and McHugh resigned three months later.

McHugh's assistant Michele Cherry was named her successor, but Cherry suffered three straight 20-loss seasons and was on course for a fourth before she resigned in the middle of the 2010–11 campaign, leading assistant Evelyn Thompson to handle head coaching duties for the remainder of the season.

On April 7, 2011, Canisius associate head coach Beth O'Boyle was named Stony Brook's fourth Division I head coach. O'Boyle went 4–26 in her first season and improved by 10 wins in each of the next two years. She won a program record 24 games in 2013–14 as Stony Brook returned to the America East Championship for the first time since 2002, but were blown out 70–46 by Albany. Stony Brook qualified for the 2014 WNIT and lost to Michigan 86–48 in Ann Arbor. The Wolverines' head coach was former Stony Brook player Kim Barnes Arico. On April 28, 2014, O'Boyle resigned to accept the head coaching position at VCU.

On June 15, 2014, Auburn assistant head coach Caroline McCombs was named as O'Boyle's successor. In McCombs' first two seasons, Stony Brook finished with 17 wins and in third place in the America East, earning bids to the WBI both times, losing to Siena in 2015 and Youngstown State in 2016. McCombs became the program's all-time winningest head coach on November 21, 2018 with her 67th win, surpassing Roberts. Stony Brook won its first game against a Power Five school by defeating Penn State 81–70 on November 25, 2018. Her first 20-win season came in 2018–19 but ended in the America East semifinals with a loss to Hartford. McCombs reached 100 career victories on January 2, 2020.

The 2019–20 season saw Stony Brook shatter program records, at one point owning a 22-game winning streak, the longest in the nation. Stony Brook defeated Pittsburgh in December for its second program Power Five victory. The Seawolves won their first America East regular season title after defeating Vermont to improve to 25–1 and 13–0 in conference. As the top seed, Stony Brook advanced to the America East Championship with a 28–3 record, set to face Maine at home, but the game was canceled a day before as the COVID-19 pandemic began to sweep through the United States. The Seawolves still earned the America East title as the highest seed remaining.

Stony Brook earned its redemption in the 2020–21 season. The Seawolves, as the second seed in the America East Tournament, earned a bye to the semifinals, routing UMass Lowell to set up a championship rematch with top-seeded Maine. On the road, Stony Brook came back from an 11-point deficit to upset Maine 64–60 and clinch its first trip to the NCAA Tournament in program history. Stony Brook lost 79–44 to Arizona in the first round. McCombs announced on April 2, 2021 that she would be leaving Stony Brook after seven years to be George Washington's new head coach.

On April 28, 2021, James Madison assistant Ashley Langford was hired to replace McCombs. In Langford's first season, Stony Brook finished 23–6 with wins over St. John's, Rutgers and Washington State. However, Stony Brook was banned from the America East tournament because the team announced it would be leaving the conference to join the Colonial Athletic Association (CAA). Stony Brook was invited to the WNIT, losing at VCU 56–48. In 2022–23, Stony Brook finished 18–13 in its first CAA season, losing to Northeastern in the second round of the conference tournament. Stony Brook won the 2023–24 CAA regular season title by going 25–3 overall and 16–2 in conference.