The VHM first opened in 1997, founded by Mark Fetter, Jay Ipson, and Al Rosenbaum. Housed in the former Education building at Temple Beth El, the museum became an attraction for school field trips. Within a few years, the museum outgrew the space at Temple Beth El, and required additional room to handle the growing number of visitors and school groups.

The Virginia General Assembly offered the American Tobacco Company Warehouse for the relocation of the museum. After restoration and reconfiguration of the building, the expanded Virginia Holocaust Museum was dedicated on Yom HaShoah, the Holocaust Day of Remembrance, 2003.

The Virginia Holocaust Museum has grown steadily since 2003, and now has an average of over 42,000 visitors each year. The VHM remains an important location for Virginia field trips, with students from over 100 middle and high schools visiting yearly.

The museum began an extensive ongoing exhibition renovation project in 2015. Much of the permanent exhibition had never been updated since opening in 2003, and the renovations serve to both update the information contained with newly uncovered facts and figures, as well as update the core exhibition space to professional standards. The VHM hopes these renovations will be completed by 2020.

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