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After graduating from law school, Thacker spent two years working in the Pittsburgh office of the law firm Kirkpatrick & Lockhart (now K&L Gates). She then worked briefly for the West Virginia Office of the Attorney General before joining the law firm King, Betts & Allen. In 1994, Thacker took a job in the United States Attorney's office for the Southern District of West Virginia, serving as an Assistant United States Attorney in the Criminal Division and handling a wide range of criminal prosecutions.
In 1999, Thacker moved to Washington, D.C. to work as a trial attorney in the United States Department of Justice's Child Exploitation and Obscenity Section. She worked there for seven years, serving as Deputy Chief of Litigation for two years and then as Principal Deputy Chief of Litigation for five years. She also was part of the team that prosecuted the first case the United States ever brought involving the Violence Against Women Act. In 2006, Thacker joined the Charleston, West Virginia, law firm Guthrie & Thomas as a partner.
In October 2017, Thacker wrote for the panel majority when it found that the Bladensburg Peace Cross memorial from World War I now violated the Constitution's Establishment Clause and ordering either its arms removed or the entire monument razed. Her judgement was ultimately reversed by the U.S. Supreme Court in American Legion v. American Humanist Association (2019).
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Thacker in 2022