Terwilliger received his Bachelor of Arts degree from the University of Virginia and his juris doctor, with highest honors, from the William and Mary School of Law.

During his time as an assistant United States attorney, he was detailed to the Senate Judiciary Committee where he served as a criminal counsel to Chairman Charles Grassley.

[6] Senators Tim Kaine and Mark Warner recommended Terwilliger to serve permanently as United States attorney.

[7] On July 13, 2018, President Donald Trump announced his intent to nominate Terwilliger to be the U.S. attorney for the Eastern District of Virginia.

[12][13] Terwilliger's father is George J. Terwilliger III, the former United States Deputy Attorney General under George H. W. Bush and United States Attorney for the District of Vermont under Bush and Ronald Reagan.