The land around Wyndham has long been home to Aboriginal people, with the region sitting along the boundary of several traditional territories. These groups, each with their own distinct languages and cultures, have shared and interacted with the land for thousands of years. These groups have come together under the name Balanggarra and have had Native Title recognised in the region.

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The Wyndham Port was first established in 1884 on the Cambridge Gulf, and plans for a town were developed after gold was discovered south at Halls Creek. Though the gold rush was short-lived and the initial town site uninhabitable, Wyndham began to grow. Cameleers from India, known as "Afghans" were vital in the movement of goods across the Kimberley in these early days. The Wyndham Meatworks operated from 1919-1985 and was the end of the road for key stock routes from stations from the east and south. The Meatworks were a key source of employment for the town and the town's economy and services grew to support it. 

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The main town site is now three miles south of the Old Port town. 

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