[2] He was the Trump administration's nominee to be Under Secretary of State for Arms Control and International Security Affairs, and he previously served as a U.S. Senate staffer and as a Department of Defense official.

[2][5][6] During the first presidential transition of Donald Trump, Billingslea headed the United States National Security Council team.

[7] In April 2017, Billingslea was nominated by President Donald Trump to become Assistant Secretary for Terrorist Financing in the United States Department of the Treasury.

His areas of focus include money laundering, terrorist financing, WMD proliferation, and other criminal and illicit activities domestically and internationally.

[2] He led specific efforts to counter threats including proliferation, terrorism, and the deceptive financial practices posed by countries such as Iran and North Korea.

"[13] Others, including the Foundation for Defense of Democracies (FDD), wrote in support of his nomination with a letter challenging all of the claims made by these other groups.

During his tenure, the FATF established new standards to govern the regulation of virtual assets (crypto-currencies) and conversion of the FATF principle that terrorist financing must be criminalized, even absent a direct tie to a terrorist act, into binding international law pursuant to UN Security Council Resolution 2462.