In addition to trolleys, the museum also operates restored subway cars, a small number of both trolleybuses and conventional buses.

[2][3] The museum was incorporated in August 1945 as the Branford Electric Railway Association (BERA), a non-profit historical and educational institution.

The Connecticut Company (or ConnCo), which operated most of the streetcar lines in the state of Connecticut, had been making plans since the early 1930s to abandon its "F" route, cutting it back in stages from its long-time terminus of Stony Creek until by April 1946 it ended in front of the post office in Short Beach, its original terminus when the line was opened for service on 31 July 1900.

Over the following year the museum moved virtually its entire collection at the time, including a number of just-retired ConnCo streetcars, onto its property via the existing and still-electrified track connection with Connecticut Company.

[4] In August 2011, Hurricane Irene caused the worst flooding in the museum's history, with water up to 2 feet deep covering the grounds and almost 90 streetcars damaged.

[8] Regular operation – proposed to take place about once a month[7] – has not yet begun (as of 2023), because the vehicles need more work (such as painting) before they are considered ready for public rides.