From 1990 to 1997, Dhillon served as an Assistant U.S. Attorney in Los Angeles, where he prosecuted major narcotics cases.

Dhillon was appointed to the United States Department of Justice's Organized Crime Drug Enforcement Task Force.

As part of the task force, he coordinated with federal, state, and local law enforcement agencies to direct investigations of violent gangs and major narcotics trafficking organizations.

In 2003, he served as chief counsel and deputy staff director of the United States House Committee on Homeland Security.

In 2006, Dhillon became the first director of the Office of Counternarcotics Enforcement at the United States Department of Homeland Security.