The idea of a crossing at the Narrows — the strait connecting Upper New York Bay to Lower New York Bay and the Atlantic — had been floating around since at least 1926, when structural engineer David B. Steinman proposed a bridge. Nothing happened. A Staten Island tunnel was proposed and aborted. Another tunnel proposal arose in the 1930s, then again in the 1940s. Staten Island remained connected to the rest of New York City only by the Staten Island Ferry. It was Robert Moses, the urban planner who remade postwar New York with an almost frightening confidence, who finally pushed the project through. Surveying began in January 1959. When it opened on November 21, 1964, it was 35 years after Steinman's original proposal.

Othmar Ammann, the Swiss-born engineer who had already designed the George Washington Bridge and the Bayonne Bridge, led the project. The numbers are large enough to require a pause: the central span is 4,260 feet, which made it the longest suspension bridge span in the world at its opening, a record it held until Britain's Humber Bridge was completed in 1981. Each anchorage contains 780,000 short tons of steel and concrete. The two towers rise 693 feet above the water. The towers are so far apart that their tops are nearly two inches farther from each other than their bases — the curvature of the Earth is a measurable variable at this scale. Roughly eight thousand workers spent five years building it.

Construction required the demolition of homes in the Bay Ridge neighborhood of Brooklyn to clear the approach. Approximately 7,000 residents were displaced, many of them from an Italian-American community whose families had lived there for generations. Their departure was not voluntary. Robert Moses, whose authority over such decisions was nearly unlimited at the time, moved forward without meaningful consultation. The bridge that now bears the name of an Italian explorer was built partly through the erasure of an Italian-American neighborhood. The community that was displaced never fully reconstituted itself.

The Verrazzano–Narrows Bridge opened on November 21, 1964, seven months after the Unisphere was dedicated at the World's Fair a few miles away in Queens. It brought Staten Island into genuine connection with the rest of the city for the first time. It carries Interstate 278 — the Staten Island Expressway and the Brooklyn–Queens Expressway — on two decks, with thirteen lanes of traffic. Every November, the New York City Marathon begins on the upper deck and proceeds across the bridge toward Brooklyn and ultimately Manhattan. From the water or from the air, the bridge's twin towers and long cables form one of the most recognizable silhouettes in the harbor.