The route that is currently the R train was built in three distinct segments. The portion that runs from 95th street, Brooklyn, up Fourth Avenue, across to Manhattan and up the Broadway line was part of the original BMT subway constructed by 1920. The portion along the Queens Boulevard line was built by the city run Independent Subway System (IND) and opened in the early 30s.

When the BMT, along with the IRT, was bought out by the city and the lines were unified in 1940, one of the first connections built between former BMT and IND trackage was the 57th street tunnel under the East River connecting the BMT Broadway line to the IND Queens boulevard line, where the current R route runs today.

When the Transit Authority introduced letter designations to the unified system, the route was called the RR (double letters designated local trains). It originally ran through the Fourth Avenue and Broadway lines as it does today, but then followed the 60th street tunnel to the Astoria Line, terminating at Ditmars as the N Train does currently. It was later changed to the current route, running through the 57 street tunnel to the Queens Boulevard line. When the MTA got rid of the double letter system in 1986, the line was renamed to just the R.

Currently the R Train runs exclusively R44-46 rolling stock, well appointed 75' cars from the early 70s featuring LED destination displays.