The 86th Street station was constructed for the Interborough Rapid Transit Company (IRT) as part of the Dual Contracts.

Unlike at most express stations, the respective pairs of northbound and southbound platforms are not connected to each other within fare control.

Following the completion of the original subway, there were plans to construct a line along Manhattan's east side north of 42nd Street.

In July 1911, the IRT had withdrawn from the talks, and the Brooklyn Rapid Transit Company (BRT) was to operate on Lexington Avenue.

[21] For over a year, community members had asked Gimbels to include an entrance into the store's basement from the subway.

[22] While the renovation took place mostly in the fare control areas, work was also done to fix the station's lighting, walls, floors, turnstiles, stairways, and token booths.

As part of the project, structural deficiencies were repaired, signage and lighting were enhanced, electrical service was upgraded, station facilities were rehabilitated, new fare arrays and a new token booth were installed, and portions of the station were upgraded to be compliant with the Americans with Disabilities Act of 1990.

[33][34] Accessibility of the entire station was proposed in August 2019 as part of the MTA's "Fast Forward" program.

[35] A request for proposals was put out on May 18, 2023 for the contract for a project bundle to make 13 stations accessible, including completing work at 86th Street.

[5]: 4  There are no crossovers or crossunders between the platforms, making this one of only two express stations in the system where free transfers between opposite directions are not possible.

The outer walls of this trough are composed of columns, spaced approximately every 5 feet (1.5 m) with concrete infill between them.

Additional columns between the tracks, spaced every 5 feet (1.5 m), support the jack-arched concrete station roofs.

[5]: 4  At the extreme southern ends of all four platforms, there are tan terracotta blocks and a darker trim line with "86TH ST" written on it in white sans serif font at regular intervals.

It consists of four different glass and etched stone mosaic murals in the shapes of huge eyes surrounded by various animals and objects.

They are located at each stop of the four staircases near the fare control areas that go down to the lower level express platforms.

[52] From the northbound fare control, there is an unstaffed turnstile bank and two staircases going up to the southeast corner of East 86th Street and Lexington Avenue.

The elevator and staircase installations are part of the construction of a luxury residential tower at 147 East 86th Street.