McCusker was nominated by President Donald Trump to become United States Principal Deputy Under Secretary of Defense in April 2017 and was confirmed on August 1, 2017.[2][3][4] In November 2019, the White House announced that McCusker would be nominated to succeed David Norquist as the Under Secretary of Defense (Comptroller).[5] On March 2, 2020 it was reported that her nomination was being withdrawn by the White House following reports that in 2019 she had warned that freezing military aid to Ukraine might not be legal.[6]
McCusker contributed to announcements in September 2019 regarding Trump's plan to divert Pentagon funds to build a wall along the U.S.-Mexico border. McCusker announced wall construction could begin as within three months on federally owned land. Construction of the wall on other government or privately owned land would commence at a later date, she noted.[10]
McCusker then sent emails to the OMB expressing concern that by withholding funds from the Ukraine, the White House was violating the Impoundment Control Act, which requires that the executive branch spend appropriations that have been approved by Congress.[13]
On June 16, 2020, she announced her resignation as Deputy Under Secretary, effective June 26.[14]