It was more difficult to build than other subway trunk lines in New York City because construction had to proceed around, over, and under existing tunnels and elevated structures.

On the south end, the express tracks used by the B and ​D trains diverge to Grand Street and the Manhattan Bridge.

A flying junction just to the south connects the local tracks of the Sixth and Eighth Avenue Lines.

[3] Since the IND typically installed express–local crossovers beyond the fronts of the station platforms, an anomaly in the track layout was created when the Chrystie Street Connection was built.

[3][7] As a result, unusual routings are required whenever a train on the Eighth Avenue Line needs to access the Manhattan Bridge.

[8][9]: 11  Other provisions for unbuilt lines exist at the mezzanine levels of the Second Avenue and East Broadway stations, where unfinished open spaces indicate where stations for the Second Avenue Subway and IND Worth Street Line, respectively, would have been built.

[3] New York City mayor John Francis Hylan's original plans for the Independent Subway System (IND), proposed in 1922, included building over 100 miles (160 km) of new lines and taking over nearly 100 miles (160 km) of existing lines.

[14] In 1924, the IND submitted its list of proposed subway routes to the New York City Board of Transportation (NYCBOT), which approved the program.

[15] Work on the core section of the IND Sixth Avenue Line, located between Fourth and 53rd Streets, was not to begin for several years.

[18] The IND started advertising bids for the section of the Sixth Avenue Line between 43rd and 53rd Streets in April 1931.

[20] The NYCBOT wanted to start work on the section between 33rd and 39th Streets first so that the engineering issues with the H&M tubes and water main could be resolved.

[22] In 1933, the New York City Board of Estimate requested a $25.5 million federal loan for the construction of the Sixth Avenue line.

[26] In May 1933, the city started widening Essex and Rutgers Streets to accommodate the future subway line underneath.

E trains, which ran from Jackson Heights, Queens to Hudson Terminal, were shifted to the new line to East Broadway.

[28] Two express tracks were built on the portion under Houston Street until Essex Street-Avenue A; the tracks were intended to travel under the East River and connect with the never-built IND Worth Street Line in Williamsburg, Brooklyn.

[29][30] In April 1935, engineers started planning in earnest for the Midtown section of the Sixth Avenue Line.

[32][33] Mayor Fiorello H. La Guardia broke ground for the Sixth Avenue subway at Bryant Park on March 23, 1936.

[37] The next month, the George A. Flynn Corporation received a contract for the construction of the section between 47th and 53rd Streets.

[38] The Arthur A. Johnson Corp. and Necaro Co. received the contract to build the segment between 18th and 27th Streets in January 1937.

The work largely involved cut-and-cover excavations, although portions of the subway had to be tunneled through solid rock.

[42] Builders had to use very small charges of dynamite so that they would not disrupt the H&M tunnels alongside the route, the street and elevated line above, and the water main below.

[4][48] This extension was part of the Board of Transportation's long-range program, and was estimated to cost $34.914 million as of August 1940.

[49][50][51] On April 19, 1961, ground was broken for a $22 million project to build two express tracks between the West Fourth Street and 34th Street–Herald Square stations.

[52] The express tracks were part of an $80 million subway improvement program that began with the reconstruction of the DeKalb Avenue station in Brooklyn.

[57] Construction on the section between West 19th and 31st Streets was further along: it had started in the middle of 1961, and was 60 percent complete in July 1963.

[60] The Program for Action, a series of subway and commuter rail expansions proposed by the MTA to then-Governor Nelson Rockefeller, included a spur of the line to the underserved Alphabet City neighborhood on the Lower East Side.

[62][63] The branch's construction was delayed in 1971 after voters blocked a bond issue, then canceled along with most of the Program's new projects after the 1975–76 New York City fiscal crisis and extreme MTA fare revenue fluctuations.

[64]: 238–243 [65] The tracks at 57th Street were originally built for a proposed extension under Central Park to Harlem.

[5] The stub-end tracks were eventually connected to the IND 63rd Street Line when the latter opened in October 1989.

The interlocking upgrades would support communications-based train control (CBTC) installation on the Queens Boulevard, Culver, and Eighth Avenue lines.