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ABSTRACT Humans have a long history of fermenting food and beverages that led to domestication of the baker's yeast,Saccharomyces cerevisiae. Despite their tight companionship with humans, yeast species that are domesticated or pathogenic can also live on trees. Here we used over 300 genomes ofS. cerevisiaefrom oaks and other trees to determine whether tree‐associated populations are genetically distinct from domesticated lineages and estimate the timing of forest lineage divergence. We found populations on trees are highly structured within Europe, Japan, and North America. Approximate estimates of when forest lineages diverged out of Asia and into North America and Europe coincide with the end of the last ice age, the spread of agriculture, and the onset of fermentation by humans. It appears that migration from human‐associated environments to trees is ongoing. Indeed, patterns of ancestry in the genomes of three recent migrants from the trees of North America to Europe could be explained by the human response to the Great French Wine Blight. Our results suggest that human‐assisted migration affects forest populations, albeit rarely. Such migration events may even have shaped the global distribution ofS. cerevisiae. Given the potential for lasting impacts due to yeast migration between human and natural environments, it seems important to understand the evolution of human commensals and pathogens in wild niches.