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Previous comparative and experimental evolution studies have suggested how fungi may rapidly adapt to new environments, but direct observation of in situ selection in fungal populations is rare due to challenges with tracking populations over human time scales. We monitored a population of Penicillium solitum over eight years in a cheese cave and documented a phenotypic shift from predominantly green to white strains. Diverse mutations in the alb1 gene, which encodes the first protein in the DHN-melanin biosynthesis pathway, explained the green to white shift. A similar phenotypic shift was recapitulated with an alb1 knockout and experimental evolution in laboratory populations. The most common genetic disruption of the alb1 genomic region was caused by putative transposable element insertions upstream of the gene. White strains had substantial downregulation in global transcription, with genetically distinct white strains possessing divergent shifts in expression of different biological processes. White strains outcompeted green strains in co-culture, but this competitive advantage was only observed in the absence of light, suggesting that loss of melanin is only adaptive in dark conditions. Our results illustrate how fermented food production by humans provides opportunities for relaxed selection of key fungal traits over short time scales. Unintentional domestication of microbes by cheesemakers may provide opportunities to generate new strains for innovation in traditional cheese production.