The clapboard-sided, Georgian-Federal-style building, constructed on land donated by the Flatbush Reformed Dutch Church, was turned over to the public school system in 1896.

Around the start of the 20th century, Brooklyn experienced a rapidly growing population, and the original small school was enlarged with the addition of several wings and the purchase of several nearby buildings.

The original Academy building, which still stands in the courtyard of the current school, served the students of Erasmus Hall in three different centuries.

Now a designated New York City Landmark and listed in the National Register of Historic Places, the building is a museum exhibiting the school's history.

[4] Land was donated by the Flatbush Dutch Reformed Church for the building and contributions were collected for “an institution of higher learning,” from leading citizens such as Aaron Burr, Alexander Hamilton, Peter Lefferts and Robert Livingston.

The wood-framed, clapboard-sided, Georgian and Federal style school building,[3] two and one-half stories tall with hipped roof, was opened in 1787 with 26 students.

The village evolved into a city, and started a public school system that competed with Erasmus for its student body.

The style of Erasmus Hall evolved over the years so that the most recent buildings are simpler, with less ornamentation, but retain the general characteristics of the earlier ones, giving a sense of unity to the entire composition.

The buildings, therefore, have been designed as a screen across the end of the quadrangle, shutting out the noise and confusion of Flatbush Avenue traffic, the only entrance being through the large arch under the tower, which is placed on the axis of the longer dimension of the plot.

As such the endeavor has been to design a harmonious, impressive room, in a style permeated with history and romance; a place which, of all others, will stand out clearly in the loving memory of the student in after years for his alma mater.

Its walls, columns and arches should bear the trophies won in athletic and scholastic contests, there to be preserved and handed down as part of the glorious history of the school.

The construction contract was initially supposed to run until October 1905, but revisions required by the school board for laboratories and classrooms necessitated changes in the electrical and sanitation plans and delayed the work.

This group of three buildings, including one to the north of the tower facing Flatbush Avenue, and two extending east along the northern side of the lot, comprised 31 classrooms, laboratories, study hall, music, drawing, physics, lecture and shop rooms.

In April 1924, the Board of Education approved the Bedford Avenue addition to Erasmus Hall High School.

[31] Dedicated in 1931, the base is engraved with the words: Desiderius Erasmus, the maintainer and restorer of the sciences and polite literature, the greatest man of his century, the excellent citizen who, through his immortal writings, acquired an everlasting fame.Lobbying began in 1929 for the construction of the final section, the building on the south side of the lot connecting the Bedford Avenue building with the auditorium near Flatbush Avenue.

[32] Under the supervision of the school system's then chief architect, Eric Kebbon, the five-story building was an even more simplified version of Snyder's earlier work.

It contained many classrooms, art and homemaking rooms, a girls' gym and a large library, and could accommodate 1,566 additional pupils.

A 2019 report states that "the building still needs more love but in 2017 Brooklyn Borough President Eric Adams pledged $650,000 of the capital budget for exterior restoration".