The wind-induced collapse occurred on November 7, 1940 at 11:00 AM (Pacific time), due partially to a physical phenomenon known as mechanical resonance.

The bridge was solidly built, with girders of carbon steel anchored in huge blocks of concrete. Preceding designs typically had open lattice beam trusses underneath the roadbed. This bridge was the first of its type to employ plate girders (pairs of deep I beams) to support the roadbed. With the earlier designs any wind would simply pass through the truss, but in the new design the wind would be diverted above and below the structure. Shortly after construction finished at the end of June (opened to traffic on July 1, 1940), it was discovered that the bridge would sway and buckle dangerously in relatively mild windy conditions for the area. This resonance was transverse, meaning the bridge buckled along its length, with the roadbed alternately raised and depressed in certain locations -- one half of the central span would rise while the other lowered. Drivers would see cars approaching from the other direction disappear into valleys which were dynamically appearing and disappearing.

The failure of the bridge occurred when a never-before-seen twisting mode occurred, from winds at a mild 40 MPH. This is called a torsional, rather than longitudinal, mode (see also torque) whereby when the left side of the roadway went down, the right side would rise, and vice-versa, with the centerline of the road remaining still. Specifically, it was the second torsional mode, in which the midpoint of the bridge remained motionless while the two halves of the bridge twisted in opposite directions.