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Inniskillin was founded by Donald Ziraldo and Karl Kaiser and saw its beginnings in 1974. Before embarking on the Innskillin project, Ziraldo was running a grapevine nursery and Karl Kaiser, a trained chemist, was a home wine maker. The first vines were planted in 1974, and since the duo had the ambition to make better-quality wines, their vineyard was planted with traditional European grape varieties, of the Vitis vinifera species, chosen from those cultivated in colder European regions. Their first vineyard, of 32 acres (13 ha) was planted with Riesling, Chardonnay and Gamay.
At that time the wine industry in the Niagara consisted of five bulk wineries growing American ("non-vinfiera") vines, and no winery licenses had been issued since 1929. Inniskillin's license in 1975, which Ziraldo successfully lobbied for, was therefore the first post-prohibition license issued in the region. The company Inniskillin Wines was formally incorporated in July 31, 1975, and the first harvest occurred three years after their first vineyard was planted, in 1977. While waiting for their V. vinifera vines to yield grapes, they produced some wine from hybrid grapes. In 1978, Inniskillin moved to its present location on the Brae Burn Estate. An existing 1920s barn, thought to have been inspired by architect Frank Lloyd Wright, was restored for the winery's use, and has become something of a landmark.
The two founders of Inniskillin practiced a division of labour. Kaiser handled the winemaking, and Ziraldo handled the marketing and was president of the company. Ziraldo was also instrumental in creating the Vintners Quality Alliance (VQA) and was the organisation's first chairman.
In 1992, Inniskillin Wines merged with Cartier wines (one of the old wineries of the region, founded in 1889) to form Cartier Inniskillin Vintners Inc. In 1993, Cartier Inniskillin Vintners Inc. merged with T.G. Bright & Co. Limited (founded in 1874 as the Niagara Falls Wine Company) under the name Vincor International Inc. Inniskillin wines continued as a subsidiary of Vincor, with the wines labelled as before and Ziraldo and Kaiser in their old roles.
In 1994, Inniskillin started activities at a subsidiary winery in Okanagan, British Columbia, under the name Inniskillin Okanagan. After that, the original winery was referred to as Inniskillin Niagara. This winery was started in collaboration with First Nation locals, the Okanaqueen Tribe of the Inkameep people, which kept vineyards on their land and supplied grapes to Inniskillin Okanagan. In 1996, Inniskillin expanded their Okanagan activities by buying an existing winery in Okanagan, Okanagan Vineyards, as well as the Dark Horse Vineyard.
In April 2006, Constellation Brands bought Inniskillin's parent company Vincor International Inc., which became Vincor Canada. Later that year Karl Kaiser went into retirement, but stayed on as a consultant for Inniskillin's ice wine activities, and Ziraldo left the winery and his position as president.