The route that is the current D Train began as the Brighton Line, a mid 19th century tourist railway through Southern Brooklyn that took holiday makers to the resort at Coney Island. This is the portion of the currentD route from approximately Church Ave. to near Brighton Beach.

Eventually, the Brighton Line was acquired, along with the rest of the South Brooklyn railways, by the Brooklyn Raid Transit Corporation, or BRT, later the Brooklyn Manhattan Transit corporation, or BMT. The BMT operated the vast elevated transit network in Brooklyn at the turn of the century, and was one of the two private companies, along with the Interboro Rapid Transit, that built the initial portions of the New York City subway and whose systems, along with the city built Independent, were consolidated to form the subway system as we know it.

The BMT initially tied the Brighton line into the rest of its network through the route of the current Franklin Avenue Shuttle from Parkside to Fulton Avenue, where it connected to the Fulton Avenue Elevated and service to Manhattan via the Brooklyn Bridge. The Brighton line was also extended at the southern end to the terminal at Stillwell Avenue.

By 1920 the BMT had already completed one subway route between south Brooklyn and Manhattan, the line that runs up Brooklyn's Fourth Avenue, across the East River on one of two routes, and up Broadway (today's R Train). Several other older railways from Southern Brooklyn were connected into this line for through service and could run either through the Montague Street tunnel to the Broadway line in the financial district, or over the south side Manhattan Bridge tracks to Canal Street, where they joined it. The two Manhattan access lines, via the bridge and via the tunnel, diverged at De Kalb Avenue.

Later, in the Dual Contracts era of subway construction, in which the city planned the routes of the BMT and IRT, the BMT tied the Brighton Line into this De Kalb Avenue network of Manhattan access with the subway under Flatbush Avenue. There was now a route identical to today's D train in the portion from Brighton Beach to the Manhattan Bridge. At the time trains from Brighton went either through the tunnel or over the bridge to the Broadway line, neither of which they do today.

In the late 20s and early 30s, the city built its own Independent system to compete with the BMT and IRT. The Independent, or IND, included the rest of the route of today's D, a trunk line under Sixth Avenue in Manhattan connecting to a line under Central Park West and the Concourse Line under the Grand Concourse in the Bronx. The express tracks under Sixth Avenue were not yet built and the line was not yet connected to the Manhattan Bridge.

In 1940 the city consolidated the three formerly separate transit systems and began the task of unifying them. The final step in the evolution of the route of today's D was the Chrystie Street connection, completed in 1967, which connected tracks on the north side of the Manhattan Bridge to the new Sixth Avenue express tracks. This was a major step in the unification of the system. Trains from Brighton and under Flatbush could now cross the Manhattan Bridge and continue via Sixth Avenue to Central Park West and the Concourse line, as they do today. When letters were introduced for the new lines, this route was assigned to the B Train with the 'QB' running as an express route.

Eventually the Brighton/Flatbush/Sixth Avenue route was reassigned to the D, and when double letters were eliminated in 1986 the QB became the Q Train.

The D line currently runs exclusively R68 stock, disgusting 75' cars from the early 80s with mirrored interiors.

There are major changes in store for the D. Construction will close the south side tracks on the Manhattan Bridge, and the D will likely be rerouted to the north side tracks, which connect to Canal Street and the Broadway line. It will probably run in two segments, a southern one as far as 34th Street on the Broadway line, and a northern one including the Upper West Side and Bronx portions.