The bridge, which opened on July 3, 1937, connects the Rockaway Peninsula in Queens, with Flatbush Avenue to Floyd Bennett Field, Belt Parkway, and the Marine Park neighborhood in Brooklyn.

With its distinctive twin towers (which house the vertical-lift machinery), the bridge has become an iconic landmark and symbol of the Rockaways.

The operation of this bridge includes the maintenance of the Marine Parkway from the toll plaza to Jacob Riis Park.

[5] In February 1934, the New York State Assembly introduced a bill to build a $10 million bridge connecting Flatbush Avenue in Brooklyn to the Rockaway Peninsula in Queens.

[6] The United States Department of War approved the Marine Parkway Authority's request to construct a bridge over Rockaway Inlet in December 1935, although some members of the War Department preferred a tunnel under the inlet so as to not impede marine traffic.

The existing steel-grated roadway deck on the lift span was replaced with a new steel grating.

[36] In addition, the elevators and electrical systems in the two towers were replaced, and new variable message signs and traffic control devices were installed on the bridge, approach roadways, and toll plaza.

[38] Part of the crash of American Airlines Flight 587 in 2001 was filmed from a tollbooth camera on this bridge.

[17]: 65  The main part of the Marine Parkway Bridge consists of three spans with an aggregate length of 1,500 feet (460 m).

When the Marine Parkway Bridge is "open", the center span can be raised to a height of 140 feet (43 m) to allow vessels to pass beneath the roadway.

[33] As of August 6, 2023[update], drivers pay $5.60 per car or $4.71 per motorcycle for tolls by mail/non-NYCSC E-Z Pass.

E-ZPass users with transponders issued by the New York E‑ZPass Customer Service Center pay $2.60 per car or $2.17 per motorcycle.

[42] The tollbooths for the Marine Parkway Bridge were configured to collect tolls electronically from E-ZPass transponders in 1996.

Instead, cameras and E-ZPass readers are mounted on new overhead gantries manufactured by TransCore[44] near where the booths were located.

[49] On April 10, 1957, a gate for the Marine Parkway Bridge's drawbridge span was being lowered when it hit a bus, injuring four passengers.