Desire for a bridge at this location dates back to 1889 with a Northern Pacific Railway proposal for a trestle, but concerted efforts began in the mid-1920s. The Tacoma Chamber of Commerce began campaigning and funding studies in 1923. Several noted bridge architects, including Joseph B. Strauss, who went on to be chief engineer of the Golden Gate Bridge, and David B. Steinman builder of the Mackinac Bridge, were consulted. Steinman made several Chamber-funded visits culminating in a preliminary proposal presented in 1929 but by 1931 the Chamber decided to cancel the agreement on the grounds that Steinman was "not sufficiently active" in working to obtain financing.

The road to Tacoma's doomed bridge continued in 1937, when the Washington State legislature created the Washington State Toll Bridge Authority and appropriated $5,000 to study the request by Tacoma and Pierce County for a bridge over the Narrows.

From the start, financing was the issue; revenue from tolls would not be enough to cover construction costs. But there was strong support for a bridge from the U.S. Navy, which operated the Puget Sound Naval Shipyard in Bremerton, and from the U.S. Army, which ran McChord Field and Fort Lewis in Tacoma.

Washington State engineer Clark Eldridge came up with a preliminary, "tried and true conventional bridge design," and the toll bridge authority requested $11 million from the federal Public Works Administration (PWA). But, according to Eldridge, prominent "Eastern consulting engineers" — led by New York engineer Leon Moisseiff — petitioned the PWA to build the bridge for less.

Preliminary construction plans had called for 25-foot-deep (7.6 m) girders to sit beneath the roadway and stiffen it. Moisseiff, respected designer of the famed Golden Gate Bridge, proposed shallower supports — girders 8 feet (2.4 m) deep. His approach meant a slimmer, more elegant design and reduced construction costs. Moisseiff's design won out. On June 23, 1938, the PWA approved nearly $6 million for the Tacoma Narrows Bridge. Another $1.6 million was to be collected from tolls to cover the total $8 million cost.

The wind-induced collapse occurred on November 7, 1940, due to a physical phenomenon known as mechanical resonance. From the account of Leonard Coatsworth, a driver stranded on the bridge during this event:

Just as I drove past the towers, the bridge began to sway violently from side to side. Before I realized it, the tilt became so violent that I lost control of the car... I jammed on the brakes and got out, only to be thrown onto my face against the curb... Around me I could hear concrete cracking... The car itself began to slide from side to side of the roadway.

On hands and knees most of the time, I crawled 500 yards [450 m] or more to the towers... My breath was coming in gasps; my knees were raw and bleeding, my hands bruised and swollen from gripping the concrete curb... Toward the last, I risked rising to my feet and running a few yards at a time... Safely back at the toll plaza, I saw the bridge in its final collapse and saw my car plunge into the Narrows.

The final destruction of the bridge was recorded on film by Barney Elliott, owner of a local camera shop. The Tacoma Narrows Bridge Collapse (1940) is preserved in the U.S. National Film Registry, and is still shown to engineering, architecture, and physics students as a cautionary tale.

No human life was lost in the collapse of the bridge. Theodore von Karman reported that the State of Washington was unable to collect on one of the insurance policies for the bridge, because its insurance agent fraudulently pocketed the insurance premiums. The agent, Hallett R. French who represented the Merchant's Fire Assurance Company, was charged with grand larceny for withholding the premiums for $800,000 worth of insurance. The bridge, however, was insured by many other policies that covered 80% of the $5.2–million structure's value. Most of these were collected without incident.

On November 28, 1940, the U. S. Navy's Hydrographic Office reported that the remains of the bridge were located at geographical coordinates 47°16′00″N, 122°33′00″W, at a depth of 180 feet (55 m).