The bridge is named for Millard Tydings (1890–1961), a longtime political figure in Maryland and a U.S. Senator from 1927–1951. It was built between January 1962 and November 1963 between bluffs high above the river valley, and is posted with warning signs "Subject to Crosswinds." It was dedicated, along with the highway it carries, by John F. Kennedy on November 14, eight days before the U.S. president was assassinated in Dallas, Texas. The next year, the highway was renamed the John F. Kennedy Memorial Highway.
It is one of eight toll facilities operated by the Maryland Transportation Authority. The toll, levied on northbound traffic only, is $8.00 for two-axle vehicles as of July 1, 2013; larger vehicles pay another $8 per additional axle.
The bridge was closed during Hurricane Sandy on October 30, 2012, perhaps the first time it was ever shut down.