The Criminal Investigation Unit handles all felony crimes, death investigations, domestic incidents that involve felonies, missing person reports, internal investigations, and employee background checks for all employees and contracted workers within the agency. The Unit also provides assistance to local police agencies and fire departments in Oneida County, including the cities, villages, and towns. The Criminal Investigation Unit encompasses the Investigations Section, Warrants Section, Backgrounds Section, and Forensics Section.

The Criminal Investigation Unit is directed by a Lieutenant and three Sergeants and manned by several Investigators. Investigators are selected from the ranks of Uniform Deputy Sheriffs. To become an Investigator, a Deputy Sheriff must have a minimum amount of on-the-job experience, must display an above-average knowledge of the law and its process, and must have a proven ability to initiate, document, and conclude an investigation. An Investigator works all shifts, weekends, and holidays and is subject to callback at any time.

Criminal Investigation Unit Investigators work closely with many local, state, and federal agencies in addition to the county's city, village, and town police agencies:

The relationships formed with these agencies aid the Unit in successful case investigation, closure, and prosecution, which ultimately leads to conviction and appropriate penalties for criminal offenders.

The Unit also has ties with the Federal Terrorism Task Force in Syracuse, New York, and is part of the Homeland Security Network for Oneida, Madison, and Herkimer counties. These partnerships developed as a response to the 9/11 terrorist attacks, and the partnerships have proved instrumental in providing a smooth flow of important information from the federal level to the local level.