The Herkimer first opened in 1895 as the Hotel Herkimer, at the corner of South Division Avenue and Goodrich Street. The hotel expanded in 1905 and later became part of the Milner Hotel chain. In 1995, the former hotel was converted into 122 affordable studio and single-room-occupancy apartments.

In 2013 and 2014, Dwelling Place led a major renovation that reshaped the building for a new era of housing. The original 122 small rooms became 55 one-bedroom apartments, while historic features—including the brick exterior, vaulted ceilings, carved banisters, woodwork, atriums and skylights—were restored. Today, Herkimer Division Apartments provides permanent supportive housing for people and families experiencing or at risk of homelessness, as well as people with disabilities.