Captain Cook sighted the entrance to Foveaux Strait during his circumnavigation of the South Island in March 1770, but thought Stewart Island was joined to the mainland. The strait's European discoverer was Owen Folger Smith, who found it in 1804. It is named after Joseph Foveaux, Lieutenant-Governor of New South Wales in 1808–1809.
Foveaux Strait is home to the Bluff oyster fishery, the oysters are harvested by a fleet of dredging boats - mostly operating from Bluff Harbour in the South Island - between March and August each year. Oystering began on Stewart Island during the 1860s, and gradually moved into the strait with the discovery of larger oyster beds there in 1879.
The strait is a rough and often treacherous stretch of water. In 2006, six muttonbirders died when their trawler sank while returning to Bluff. From the years 1998 to 2012 there were a total of 23 fatalities in the Strait.
John van Leeuwen swam it on 7 February 1963, in a time of 13 hours 40 minutes.