Construction on the segment of the line that includes Union Street started on December 20, 1909, and was completed in September 1912.

The station opened on June 22, 1915, as part of the initial portion of the BMT Fourth Avenue Line to 59th Street.

[12][13] Though the Transit Commission ordered the BMT to lengthen these platforms in September 1923, no further progress was made until February 16, 1925, when the New York City Board of Transportation (NYCBOT) commissioned its engineers to examine platform-lengthening plans for this and eleven other stations along the Fourth Avenue Line.

[3] The Fourth Avenue station was constructed as part of the Culver (South Brooklyn) Line of the Independent Subway System (IND).

[25][26] A free transfer point was established between the two stations on May 28, 1959, to compensate for the loss of through Culver service via the Fourth Avenue Line.

[28] In the 1960s, the NYCTA started a project to lengthen station platforms on its lines in Southern Brooklyn to 615 feet (187 m) to accommodate 10-car trains.

[4] On July 14, 1967, the NYCTA awarded a contract to conduct test borings at eleven stations on the Fourth Avenue Line, including Ninth Street, to the W. M. Walsh Corporation for $6,585 (equivalent to $60,172 in 2023) in preparation of the construction of platform extensions.

The latter change, which was also made to 15 other stations on the BMT Broadway and Fourth Avenue Lines, was criticized for being dehumanizing.

The NYCTA spokesman stated that the old tiles were in poor condition and that the change was made to improve the appearance of stations and provide uniformity.

[32] In 2007, the Metropolitan Transportation Authority (MTA) announced a three-year renovation project of the elevated Culver Viaduct.

For Phase 2A of the project, a temporary platform was built over the southbound express track to allow northbound trains to stop at the station.

For Phase 3A a temporary platform was built over the northbound express track to allow southbound trains to stop.

As part of the project, the arch bridge over Fourth Avenue was restored with the elimination of billboards and the removal of paint over the windows.

[38][36] As part of its 2025–2029 Capital Program, the MTA has proposed making the station wheelchair-accessible in compliance with the Americans with Disabilities Act of 1990.

[47][48] The station has a crew quarters structure over both platforms which is constructed of buff brick with evidence of covered windows.

[45]: 4 This station's fare control area is at street level underneath the platforms and tracks and built within the viaduct's concrete structure.

Both entrances have their original lit-up IND "SUBWAY" sign while mosaic direction tiles reading "To Coney Island" and "To Manhattan" are in the mezzanine.

[45]: 5 The western fare control area has a single staircase going down to the extreme south end of the Bay Ridge-bound platform of Ninth Street on the BMT Fourth Avenue Line.

[23] 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.

[52][53] 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.

[56][19] 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.

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

[6]: 854 [61] The walls were intended to improve ventilation, as passing trains would push air forward, rather than to the sides of the tunnel.

The one on the Manhattan-bound platform has a turnstile bank, token booth, and one staircase going up to the northeast corner of Ninth Street and Fourth Avenue.