The line that is now the F train came into being gradually. The initial segment was the current Culver portion, from Ditmas Ave. to Coney Island in South Brooklyn. It was built in the 19th century to take vacationers to the resorts at Coney. The Culver Line made its way into the hands of the Brooklyn Rapid Transit (BRT), later the Brooklyn Manhattan Transit (BMT), the holding company that owned and operated the network of elevated commuter railways throughout the city and later borough of Brooklyn. A connection was built from the northern end of the Culver line at Ditmas Ave. running west along 37th street to Fifth Avenue and into the Fifth Avenue elevated tracks which ran north through Park Slope and into the BRT network of elevateds that eventually made its way over the Brooklyn Bridge to Manhattan. Now the Culver line was part of a commuter railway. After the BRT completed the Fourth Avenue subway south through Brooklyn in the early teens (part of today's B, N, and R trains), the connection along 37th street was extended to Fourth Avenue and tied into the subway for additional service to downtown Brooklyn and Manhattan.

When the city built the Independent subway system (IND) lines in the early 1930s, the rest of the route that would become the F train was built. The section from Church Ave. to Bergen was part of the Crosstown Line (the current G Train) but was soon connected between Bergen and Jay Street for service into Manhattan. The section from Jay Street through the Rutgers Street tunnel under the East River to Manhattan, the trunk line up Sixth Avenue, the 53rd Street Tunnel back under the East River, and the Queens Boulevard trunk line all the way through Queens to the current end at 179th st. were also completed as a large part of the original IND construction. The elevated section over the Gawanus Canal from Fourth Avenue to Caroll was the only elevated portion of the Independent system as originally built, and still contains the highest elevated trackage and highest station on the subway system.

After the city unified the competing transit systems in 1940, the F Train as we know it now began to take shape. The short connection between the Culver portion at Ditmas and the Independent portion at Church Ave. was made and the now obsolete part along 37th street from Ditmas to 4th Ave. was reduced to a shuttle and torn down altogether in 1975. The moniker 'F' was applied to the current line sometime around then and it assumed its present form.

In 1979, the MTA instituted the color pattern we recognize today and the F joined the 'orange' family of trains, so grouped because they run down 6th Avenue together.

There are unused express tracks that diverge from the local tracks between Jay Street and Bergen, run under the local tracks to Caroll, run beside the local tracks to 7th Avenue, and then diverge and follow a separate tunnel to Church. The express tracks have never been in regular service, although occasionally they are used to perform maintenance on the local tracks.

Currently (2001) the F line runs only R44-46 rolling stock, characterized by well appointed cars of 75' length that were built in the early 1970s. The cars have an LED display that still says '6th Ave - Culver Local' on Coney Island bound trains.