The Culver Line's express tracks run via a separate routing underneath Prospect Park and are not visible from the platforms.

[7][8] Upon the station's completion, it served Windsor Terrace, a mostly residential area with brownstones and row houses occupied by European immigrants.

[7] In 1937, the connection to the IND Crosstown Line opened and GG (later renamed the G) trains were extended to Church Avenue, complementing the E. In December 1940, after the IND Sixth Avenue Line opened, E trains were replaced by the F, and the GG was cut back to Smith–Ninth Streets.

[10][11] In November 1967, the Chrystie Street Connection opened and D trains were rerouted via the Manhattan Bridge and the BMT Brighton Line to Coney Island.

[14][6] Express service between Bergen and Church ended in 1976 due to budgetary concerns and passenger complaints, and the GG, later renamed the G, was again terminated at the Smith–Ninth Streets station.

[17] In July 2019, the MTA revealed plans to restore express service on the Culver Line between Jay Street and Church Avenue.

The two express tracks of the line run along a separate, more direct alignment under Prospect Park, and are not visible from this station.

[21] Both trackside walls have an orange-yellow trim line with a medium red-brown border with small black and white "15TH ST" tile captions below it at regular intervals.

[3]: 4  The ceiling of the platform level is held up by H-shaped piers located every 15 feet (4.6 m), which support girders underneath the mezzanine.

[3]: 3 The narrow mezzanine is full-length, sparsely decorated with plain tiling typical of the IND, and allows out-of-system walking from one end to the other.

The station's only token booth and bank of regular turnstiles is located between the south and center fare control areas, and there are additional communications rooms on the southern end of the mezzanine.

[3]: 5 Several dream sequences in the film Pi, which take place in an empty generic-looking New York City Subway station, were shot at 15th Street–Prospect Park.