The Division began operation in 1934, under United States Attorney General Homer Stille Cummings, who charged it with primary responsibility for supervising all federal litigation involving internal revenue (following an executive order from President Franklin Delano Roosevelt).

Among the Division's duties are: In August 2013, the Justice Department announced their Swiss bank program, which "provides Swiss banks an opportunity to come forward, cooperate, disclose their illegal conduct, and be eligible for non-prosecution agreements -- or in egregious cases, deferred prosecution agreements.

"[1] The offshore voluntary disclosure program is for individual taxpayers to come forward and pay owed taxes on undisclosed income.

[2] On February 4, 2020, President Donald Trump nominated Richard E. Zuckerman as Assistant Attorney General to head the Tax Division,[3] a post that requires Senate confirmation.

He succeeded Caroline D. Ciraolo, former Acting Assistant Attorney General, who left the Tax Division in January 2017.