The Q train runs the length of the entire line from Coney Island–Stillwell Avenue to the Manhattan Bridge south tracks.

From 1903 to 1908, all of the original line's grade crossings were eliminated; This project also widened the line from two to four tracks from Church Avenue to Sheepshead Bay; From 1918 to 1920 the portion of original open-cut right-of-way from Church Avenue to Prospect Park station was widened to four tracks and a new subway alignment was built north of the Prospect Park station.

Seeking a new route for its excursion business and its local trade in communities along the way, it formed an agreement with the Kings County Elevated Railway to connect to its Fulton Street Line, which gave access to the new Brooklyn Bridge and Manhattan passengers.

A series of mergers and leases put the Brighton Beach Line in the hands of the Brooklyn Rapid Transit Company (BRT), a holding company which eventually controlled most of the rapid transit, streetcar, and bus lines in Brooklyn and part of Queens.

The original line was a two-tracked high-speed surface steam railroad operating from Bedford Station, at Atlantic Avenue near Franklin Avenue in the City of Brooklyn, at which point it made a physical connection to the Long Island Rail Road's Atlantic Branch.

From Bedford the line ran on a surface private right-of-way several blocks south to Park Place, which it crossed at grade, and then in an open cut with street overpasses through what is now Crown Heights and Flatbush, as far as Church Lane (now Church Avenue) in the Town and Village of Flatbush.

From the end of that original cut south of Church Avenue, the line was wholly rebuilt as a four-track railroad with express and local stations to a point south of Neptune Avenue at the border of Coney Island, continuing along its original right-of-way to Brighton Beach station.

The separation of the railroad grade allowed the line's trolley wire north of Sheepshead Bay to be replaced with ground-level third rail.

[3] The work by the BGCEC left the line between Park Place and Church Avenue in substantially its original condition from steam railroad days.

[4]: 2 The St. Felix Street and Flatbush Avenue Connection opened on August 1, 1920, providing direct service between the Brighton Line and midtown Manhattan.

This service was variously known as Franklin–Nassau and as the Coney Island Express, but its popular name was the "Sunny Sunday Summer Special," because it was only supposed to operate as needed on the hottest beach-going days.

During the era of route contraction from 1940 to about 1975, the Franklin Avenue Shuttle seemed a prime candidate for abandonment; its physical structure had been allowed to deteriorate and its service steadily curtailed.

[7] On June 16, 1964, Mayor Robert F. Wagner Jr. approved the award of a $2,283,933 contract for the second phase of work to extend platforms along the Brighton Line.

[8][9] Between April 26, 1986, and October 26, 1986, service was disrupted due to track repairs and other construction work along the line.

The Coney Island-bound platforms at Avenue U and Neck Road were closed for rebuilding and all southbound trains ran on the express track from Kings Highway to Sheepshead Bay.

[15] Over the next two weeks, temporary platforms were placed on the Manhattan-bound express track at Kings Highway and Avenue J for southbound service.

The Manhattan-bound platforms were closed for rebuilding until October 25 and all northbound trains operated on the express track from Sheepshead Bay to Kings Highway.

On September 27, the Manhattan-bound platforms of those three stations as well as Avenues H and M, which were then being bypassed, began rehabilitation and all northbound service was directed to the express track until Cortelyou Road.

The Chrystie Street Connection opened in late 1967, and almost all Brighton Line trains were removed from Broadway.

The Q and QB were both combined with the D on the IND Sixth Avenue Line, running express during the day and local at other times.

The daytime QT local was combined with the Jamaica local and express (then #15) to form the QJ, running through the tunnel to the BMT Nassau Street Line, which also replaced the limited rush hour Brighton “Bankers’ Specials” to Nassau Street.

The only Brighton-Broadway service was a new QB, with a limited number of runs in the peak direction at rush hours on the local Brighton and express Broadway tracks.

In 1985, the QB was renamed Q as the subway eliminated the double letter naming system for local routes.

Because of the concurrent track and infrastructure repairs on the Brighton Line, express service was suspended for two years.

D service in Brooklyn was suspended during these hours; the Q replaced it, running local to Stillwell Avenue and via the Montague Street Tunnel and Broadway Express.

The Prospect Park station contains a cross-platform interchange with the BMT Franklin Avenue Line, which is used by the S train.

The line features slightly sloped and capped reinforced concrete walls, as well as cut-and-cover tunnels underneath cross-streets.

Past Newkirk Plaza the line continues in an open cut, then begins to rise to street level at the north end of Avenue H station.

Both lines then stop at the West Eighth Street–New York Aquarium station, a double-level steel structure with two tracks on each level.