John Cutter started his career with the New York City police in 1980 as a NYC Housing police officer. In 1995, when the housing police department merged with the NYPD, Cutter continued his role as a commanding officer within the Detective Bureau. In 2001, Cutter was asked by the NYPD Commissioner to develop and implement a new unit within the intelligence division known as the criminal intelligence section. On September 11, 2001, the focus of the Criminal Intelligence Section shifted to terrorism. As the commanding officer, Criminal Intelligence Section, Chief Cutter oversaw all counter-terrorism related activities within the Intelligence Division. He retired from the NYPD in 2004.