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The Vermont Department of Public Safety was created on July 1, 1947. That year also marked the beginning of what is now called the Vermont Forensic Laboratory. The first laboratory area was a photographic laboratory constructed within the Identification and Records Division of the Vermont State Police at the original DPS Headquarters in the Redstone building in the City of Montpelier.

The first evidentiary examinations were conducted within a year. They included firearms comparisons and glass fracture matches. Over the next 20 years, the laboratory grew to provide a full range of fingerprint, firearms and photographic related evidentiary examinations. However, most chemistry related examinations were conducted by out-of-state labs. During this time period, the laboratory was known as the Vermont State Police Crime Laboratory. The personnel at that time were all sworn officers. A special budget appropriation in the 1969-1970 biennium provided for the beginning of a forensic chemistry section. Two civilian scientists were hired to start the unit. Additional funding was obtained through federal grants to purchase laboratory equipment and to construct a versatile Mobile Crime Laboratory. Laboratory services, offered free of charge to Vermont law enforcement agencies, brought workload demands which soon resulted in a significant backlog. An inferior facility added to this problem. The relocation of Department Headquarters to the Waterbury State Complex in the town of Waterbury in 1983 provided a satisfactory facility for the Laboratory.

In 1988, all positions in the laboratory were converted to civilian positions. State Troopers, who had been performing evidentiary examinations in the Firearms & Toolmark, Latent Fingerprint and Photography sections, returned to police duty in the field. The only remaining sworn position in the laboratory was the director's position, filled by a State Police captain.

On January 1, 1995, another major reorganization occurred. The Department of Public Safety formed the Division of Criminal Justice Services, formerly the Support Services Division. The laboratory's name changed from the Vermont State Police Crime Laboratory to the Vermont Forensic Laboratory. 

On May 1, 1998, the first civilian director of the Vermont Forensic Laboratory was appointed with a State Police lieutenant assigned to the laboratory as the assistant director. In December of the following year, the Vermont Forensic Laboratory became an ASCLD accredited laboratory through ASCLD-LAB (American Society of Crime Laboratory Directors-Laboratory Accreditation Board).  The laboratory has retained its accreditation status through five additional accreditation cycles in 2004, 2009, 2015, 2019, and 2023. The VFL is now accredited by ANAB for most of the services provided. Also in 2009, the laboratory became completely staffed by civilians.