It has a sheltered concrete elevated platform that stands in the shadows of the original station, which was accessible from the ends of Maxwell, Audrey, and Hamilton Avenues.

There was also a large pier built to facilitate the loading of passenger cars onto a short-lived ferry to Wilson's Point in South Norwalk, Connecticut that is now owned by the Flowers Oyster Company.

[6] On June 24, 1889, the Oyster Bay Extension Railroad, a subsidiary of the Long Island Railroad, extended the terminus of its rail line from Locust Valley to Oyster Bay and constructed this beautiful Victorian train station on land donated by Col. Robert Townsend.

This ferry, called the Cape Charles would take passengers to Connecticut where the railways would be connected to the Housatonic Railroad and continue on to Boston.

Inside the station, a large fireplace and tiled hearth were added, and on the exterior a special stucco was used that contained real oyster shells.

There are three cab simulators, each donated to the museum by the Long Island Rail Road from their Hillside Maintenance Facility, based on the M1, M7, and DE30AC, that visitors can enter and explore.

[10] As of October 2024, volunteers were able to restore and get the LIRR M7 Simulator running with Train Sim World software, used with special permission from Dovetail Games.

Three new yard tracks have been built, a classic LIRR "Ping Pong" Coach, originally used on the Knox and Kane Railroad in Pennsylvania, has been undergoing extensive restoration, and most notably, former Long Island Rail Road G5s 4-6-0 #35 has been the main focus of the museum's work, with recent activity and fundraising for the repair of the locomotive’s parts.

A GE 25 Ton Diesel Switcher, formerly LIRR #398, has been restored to operating condition to run the future train rides.

Oyster Bay is the location of one of few remaining Long Island Rail Road stations with an original turntable on site.