Huron was laid down on 1 June 1969 by builder Marine Industries of Sorel, Quebec and was launched on 9 April 1971. She was officially commissioned into the Canadian Forces on 16 December 1972 and carried the pennant number 281.
As part of Silver Jubilee of Elizabeth II, Huron represented Canada in the naval review at Spithead on 28 June 1977. On 12 March 1980, she assisted the crew of the damaged freighter Maurice Desgagnes, eventually taking them off when the ship sank.
From 19 February to the 24 February 1981, Huron was used to carry out trials of the Sea Sparrow system to be added in the TRUMP refit. Later that year she carried the Governor-General Edward Schreyer on a tour of Scandinavian ports.
In the summer of 1990, Huron accompanied by HMCS Kootenay and HMCS Annapolis, visited Vladivostok, the first visit by Canadian warships to Russia since the Second World War.
Huron was sent to the Persian Gulf in winter 1991 as part of Operation FRICTION, the Canadian Forces's contribution to Operation DESERT STORM (the Gulf War) to replace her sister ship HMCS Athabaskan as flagship of the Canadian Naval Task Group. Huron arrived after hostilities had ceased and patrolled for several months before returning to Esquimalt.
Huron began a refit known as the Tribal Class Update and Modernization Project (TRUMP) in July 1993, performed by MIL-Davie Shipbuilding at Lauzon, Quebec. It was completed on 25 November 1994. At this time her classification changed from Destroyer Helicopter (DDH) to Destroyer Guided Missile (DDG).
She was then assigned to Maritime Forces Pacific (MARPAC) and was homeported at CFB Esquimalt.
Huron served on MARPAC missions protecting Canada's sovereignty in the Pacific Ocean and enforced Canadian laws in its territorial sea and Exclusive Economic Zone. Huron was also deployed on missions throughout the Pacific and to the Indian Ocean; specifically the Persian Gulf and Arabian Sea on anti-terrorism operations.
The Huron was also used in the television show Seven Days in the episode the Devil and the Deep Blue Sea playing the part of new type of US warship under the command of a female captain.
In 1993 Huron was deployed to the Adriatic Sea in support of the United Nations naval embargo of the former Yugoslavia. She then departed for her refit that began in July of that year. After completing her TRUMP refit, Huron returned to the west coast in 1995. She took part in most major naval exercises that were performed in the Pacific Ocean. On 7 September 1999, with Royal Canadian Mounted Police and personnel from Immigration Canada aboard, the warship intercepted a vessel carrying 146 Chinese migrants. The ship migrant ship was found to be unfit and Huron transported them to Esquimalt.
Despite being the most recently refitted Iroquois-class destroyer, defence cutbacks during the late 1990s saw Huron placed in mothball status due to a personnel shortage in 2000. In 2005 she was paid off from the Canadian Forces and awaited disposal at Esquimalt.
After TRUMP Refit: Displacement 5100 Tonnes (Fully Loaded), Length: 127.8 m, Beam: 15.0 m, Draught: 4.7 m, Speed 29 kts, Complement - 280 men and officers.
Intentionally sunk as an exercise target ship 14 May 2007 during Operation TRIDENT FURY, a live-fire exercise conducted by MARPAC 100 km (54.0 mi) west of Vancouver Island. The sinking was the subject of a 2007 History Television documentary "Sinking a Destroyer".