Erasmus Hall Academy was founded in 1786 and was the first secondary school chartered by the New York State Regents. The land on which the clapboard structure was constructed was donated to the school by the nearby Flatbush Reformed Dutch Church.

Originally a private boys school, it opened in 1787 with only 26 pupils. The school began admitting female students in 1801. In 1896 after decades of falling enrollment due to competition from the City of Brooklyn public schools, the trustees of Erasmus voted to donate the building to the public school system.

After this donation and the consolidation of NYC two years later, enrollment boomed and a larger space was needed. In 1904, C. B. J. Snyder, the New York City Superintendent of School Buildings, presented plans to build a large Gothic style building. Called Erasmus Hall High School, it was built in four phases between 1905 and 1940.

The original wood-frame building remains in the center of the newer building, and can be seen through the gates under the main tower on Flatbush Avenue.