The present-day line was built as two unconnected segments operated by the Independent Subway System (IND) and Brooklyn–Manhattan Transit Corporation (BMT).

The segment of the BMT line between Ninth and Ditmas Avenues remained as the Culver Shuttle until it was closed in 1975 and later demolished.

[8] Restoration of express service has been thwarted by budget shortages, passenger opposition, and a serious signal fire at Bergen Street in 1999.

[2][6][9] The issue came to a head in June 2007, when a petition for express service reached 2,600 signatures and gained media attention.

[4] The two stations sit on a massive one-mile long[16] steel and concrete viaduct which spans the Gowanus Canal between 9th and 10th Streets.

[26] Both underground options were considered expensive and impractical, and the viaduct was estimated to save $12 million in construction costs when it was selected in 1927.

At this point the Culver Line narrows to a two-track structure bearing one more station–Neptune Avenue–before curving into West Eighth Street–New York Aquarium station on Coney Island.

[34][35] The PP&CI began serving the Union Depot at 36th Street, where transfer could be made to the Fifth Avenue Elevated, on June 7, 1890, by using the Prospect Park and South Brooklyn Railroad from a junction at Parkville.

[41] At 3:00 a.m. on March 16, 1919, the first portion of the new elevated structure opened from Ninth Avenue southeast and south to Kings Highway.

[42][45][46] The line, the last of the four to Coney Island, was completed on May 1, 1920, at which time the Brooklyn Rapid Transit Company (BRT) was forced to cut the fare from ten to five cents.

[47][48] This construction tied into the existing lower level of the BMT Brighton Line east of West Eighth Street–New York Aquarium.

[6] By 1927, it was decided to build a truss bridge over the Gowanus Canal and a viaduct over Ninth Street due to cost considerations, replacing earlier plans for a deep river tunnel.

[65] On July 1, 1937, the connection to the IND Crosstown Line opened and GG trains were extended to Smith-Ninth Streets.

[62][70][71][72] A 1931 proposal had the line travel south from Smith–Ninth Streets station through Red Hook and Gowanus to Saint George Terminal.

[13][62] Taking over operations, or "recapturing", the Brooklyn–Manhattan Transit Corporation (BMT) Culver Line elevated structure in order to institute IND service to Coney Island was a high priority of New York City planners.

[13][63] The new connection would create a one-fare ride for IND passengers to Coney Island, and eliminate congestion on the BMT's Fourth Avenue Subway.

[78] 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.

[78][79] 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.

[4] On November 26, 1967, the Chrystie Street Connection opened and D trains were rerouted via the Manhattan Bridge and the BMT Brighton Line to Coney Island.

Following renovations to the station in the 1990s, the lower level was converted into storage space and is not usable for passenger service in its current state.

[2][6][89][91] In 1986, the New York City Transit Authority launched a study to determine whether to close 79 stations on 11 routes, including the segment of the Culver Line south of either Kings Highway or Avenue U, due to low ridership and high repair costs.

[92][93] Numerous figures, including New York City Council member Carol Greitzer, criticized the plans.

The study would determine how to fix the premature deterioration of structural braces, unsatisfactory drainage, and leaking expansion joints.

The petition, which gained over 2,500 signatures by June 2007 and nearly 4,000 by September, proposed to restore express service by making the Church Avenue extension of the G permanent and extending the V (eliminated in 2010) from its Manhattan terminus to Brooklyn, sharing the Rutgers Street Tunnel with the F.[2][9][10][11] The G extension was made permanent in July 2012, freeing up the express tracks formerly used to relay trains.

Relieving the congestion, would entail widening the staircases and installing ADA-required elevators that would cost approximately $10 million per station.

[6] The possibility of reopening the Bergen Street lower level was looked at as part of the study for the reintroduction of F express service; the reopening would require significant and expensive reconstruction, including making the station ADA accessible, the reconstruction of platform stairs, improved lighting and communications, waterproofing and concrete repairs, among other things.

[6] In July 2019, the MTA announced that it planned to run four rush-hour express F trains per day, two in each direction, starting in September 2019.

[109] As part of the MTA's 2015–2019 Capital Program, CBTC is being installed on the section of the line between Church Avenue and West Eighth Street–New York Aquarium, replacing 70-year old signals.

[112] To allow the CBTC project to enter its next phase, F service was suspended south of Church Avenue during most weekends starting in early 2020.

[114] In December 2022, the MTA announced that it would award a $368 million design–build contract to Crosstown Partners, a joint venture between Thales Group and TC Electric LLC, to install CBTC along the length of the G route.