The bridge first opened to traffic in 1940, replacing ferry service as the primary connection for the town of Jamestown, situated on Conanicut Island.

The Jamestown Bridge was closed to vehicular traffic on October 8, 1992, and its main span was destroyed through a controlled demolition on April 18, 2006.

Navigating around Narragansett Bay had proved troublesome since the colonial era, the first ferry operation began in 1675 introduced an alternate to the long route around Providence, Rhode Island.

The plans were well-supported and passed the Rhode Island House of Representatives by a 96-to-1 vote, and were approved by President Franklin Roosevelt.

[4] Head-on collisions on the 22-foot-wide (6.7 m) undivided bridge were reported to be common, and the steel grid pavement was noted as "treacherous" when wet.

However, the aging structure proved to be in far worse condition than previously thought, prompting officials to go ahead with removing the entire structure.On April 18, 2006, the main span of the Jamestown Bridge was brought down by Department of Transportation employee Wilfred Hernandez, using 75 pounds (34 kg) of RDX explosives and 350 shaped charges.

The demolished steel superstructure was floated away for recycling, while concrete from the bridge piers was used to create artificial reefs below the mouth of Narragansett Bay.