Wexton was a partner in the Laurel Brigade Law Group. She served as a substitute judge in Loudoun County, Virginia, and from 2001 to 2005 as an Assistant Commonwealth's Attorney. Wexton successfully prosecuted Clara Jane Schwartz for the murder of Schwartz's father, Robert Schwartz. She ran for Loudoun County Commonwealth's Attorney in 2011, narrowly losing to Republican incumbent Jim Plowman. She was elected to the Virginia Senate in 2014.
Virginia Senate
After Mark Herring, who represented the 33rd district in the Virginia Senate, won the 2013 election for attorney general of Virginia, Wexton declared her candidacy in the special election to fill the seat. The district includes northeastern Loudoun County and northwestern Fairfax County. In the Democratic primary, Wexton defeated Herndon Town Councilor Sheila Olem. In a campaign ad Wexton spoke of her experience defending victims of rape and assault and said she would "fight just as hard against tea party Republicans who would take away a woman's health care and her right to choose, even in cases of rape and incest." The Republican Party of Virginia criticized the ad, saying it compared Tea Party activists to rapists; Wexton's campaign denied the comparison. She faced Republican John Whitbeck and Republican-turned-Independent Joe T. May in the January 2014 special election, and won 53%–38%–10%. She took office on January 24, 2014, and was reelected in the November 2015 general election. After being elected to the United States House of Representatives, Wexton resigned her Virginia Senate seat on January 3, 2019.
In April 2017 Wexton announced that she would run in the Democratic primary for the 10th District. Her state senate district included much of the eastern portion of the congressional district, wrapping around Leesburg and Sterling. In June 2018 she won a six-way primary to become the Democratic nominee. In the November general election she defeated Republican incumbent Barbara Comstock with 56% of the vote to Comstock's 44%. Wexton is only the fifth person to represent the district since its creation in 1953, and the second Democrat. The first was Joe Fisher, who served from 1975 to 1981. Her victory resulted in the Democrats holding every seat based in the Washington suburbs.
Tenure
Shortly after defeating Comstock, Wexton declared her support for DC statehood, saying, "the fact that D.C. residents pay taxes and don't get any representation is absurd, and I think that we should make sure they get voting representation." DC's non-voting Congressional Delegate, Eleanor Holmes Norton, thanked Wexton for her comments. In January 2019 Wexton hung a transgender pride flag outside her office to show her support for the transgender community, saying, "The trans community has been under attack. I wanted to show my solidarity because we are talking about my friends and family." In May 2019 Wexton called for HUD Secretary Ben Carson's resignation after his House testimony that month. She tweeted, "As a former prosecutor, I take Congressional testimony very seriously. This week, Secretary Carson lied to me and to Congress. He lied again when he called me to 'clarify' his testimony. He’s proven himself to be deceitful & inept as HUD Secretary. He should resign." Wexton announced her support for voting to impeach President Trump over his request that Ukraine announce an investigation into his political rival Joe Biden. On August 23, 2019, Wexton formed a new congressional caucus to examine and promote agritourism, which she believes could bring economic and social benefits to areas like Loudoun Valley.
