[10][11][12] Though the ramp was nearly complete, including rails and signal work, construction was halted later that year because of America's entrance into World War II.

[12][13][14] When the project was restarted in 1946, completion was delayed further due to continued material shortages and a lack of rolling stock to facilitate the new service.

[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.

[7] Following the completion of the Culver Ramp in 1954,[19][20] D Concourse Express trains replaced F service to Coney Island.

[20][12] 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.

[23][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.

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

[27][28] Jack Lovelock, a 1936 Olympic gold medalist from New Zealand, fell onto the tracks at the Church Avenue station on December 28, 1949, after complaining to his wife about dizziness; he was then killed by an oncoming train.

[33] Both outer track walls have a maroon trim line with a Tuscan red border and small tile captions below them reading "CHURCH" in white lettering on a black background.

[33] During off-peak hours, the express tracks can be used for staging subway cars without interfering with normal service.

Two staircases and one elevator from each platform go up to the mezzanine, where public restrooms at the center are available and a turnstile bank provides entrance/exit to/from the station.

Outside fare control, there are two staircases facing in different directions that go up to either southern corners of Albemarle Road and McDonald Avenues.