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The black yeast of the order Chaetothyriales is notable for its ability to produce abundant quantities of DHN-melanin. While many other species are frequent causal agents of human infection, CBS 102400 lacks the thermotolerance requirements that enable pathogenicity, making it appealing for use in targeted functional studies and biotechnological applications. Here, we report the stress tolerance characteristics of , with an emphasis on the influence of melanin on its resistance to various forms of stress. We find that has a distinct stress tolerance profile that includes variation in resistance to temperature, osmotic, and oxidative stress relative to the extremophilic and pathogenic black yeast . Notably, the presence of melanin substantially impacts stress resistance in , while this was not found to be the case in . The cellular context, therefore, influences the role of melanin in stress protection. In addition, we present a detailed analysis of the genome, revealing key differences in functional genetic content relative to other ascomycetous species, including a significant decrease in abundance of genes encoding ribosomal proteins. In all, this study provides insight into how genetics and physiology may underlie stress tolerance and enhances understanding of the genetic diversity of black yeasts.