Poster notifying passengers of service changes, 1946.

The Court Street station is a two-track stub-end station, constructed as a terminus for local trains of the IND Fulton Street Line. Opened on April 9, 1936, the station was meant to northern end of the HH Fulton Street Local, and possibility a Brooklyn connection along the long proposed Second Avenue Subway. In reality the only train service that the station operated was the Court Street Shuttle, which left Court Street and traveled the three underground blocks to the nearby transfer station at Hoyt–Schermerhorn. Given the proximity to the next station, Court Street was never heavily used and the station was closed (and the shuttle service discontinued) on June 1, 1946. The station was in active use for only 10 years and just under two months. With most of its entrances sealed the station was used for various activities after 1946 including as a testing ground for station cleaning activities, as storage for transit equipment, and as a filming location for movies.

On July 4, 1976 the New York City Transit Exhibit opened in the station as part of the United States Bicentennial celebrations. The exhibit was organized by transit employees. Meant to be on display only until Labor Day of that year, the exhibit proved to be immensely popular and remained open, eventually being transformed into a permanent museum.