Construction of Highway 406 began in 1963. The first section opened between St. Davids Road and Geneva Street on December 7, 1965, followed by a southward extension to Beaverdams Road in late 1969. The route was later extended south as a super two to Merritt Road where it became Highway 58. In 1977, construction began to connect the freeway with the QEW; this was completed in late 1984. Construction on the route resumed in 1987, connecting the route with East Main Street in Welland, completed in 1995.