The Headquarters Bureau, operating twenty-four hours a day, is the largest section of the Enforcement Division. The Bureau is located at the lower level of the Criminal Courts Building, 200 Center Drive, Riverhead, New York. The Headquarters Bureau is staffed with one Captain, two Lieutenants, nine Sergeants and eighty-four Deputies. The Sergeants and Deputies work various shifts to provide 24 hours a day, 7 days per week coverage.

The six major responsibilities of the Headquarters Bureau are: transportation and security of inmates outside the Correctional Facility, operation of a feeder detention center, 24/7 perimeter security of the Sheriff's facilities, to provide general law enforcement services to the public, county agencies and support assistance to other law enforcement agencies, K-9 patrol and response, Marine Patrol of the East End of Long Island.