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<div>Over 18 million hectares of forests have been destroyed in the past two decades in Canada by the mountain pine beetle (MPB) and its fungal symbionts <i>Grosmannia clavigera</i> (<i>Gc</i>), <i>Leptographium longiclavatum</i> (<i>Ll</i>) and <i>Ophiostoma montium </i>(<i>Om</i>) (Ophiostomatales, Ascomycota). These fungal symbionts are crucial in the establishment and reproductive success of MPB by aiding in nutritional acquisition and overcoming host-tree defenses. Understanding their population structure and adaptations are important to predict their expansion pattern and to improving modeling of beetle epidemics. We investigated their genetic structures using single nucleotide polymorphisms (SNPs) and we monitored fungal growth rates at different temperatures. We found a strong north-south differentiation in their population structure that is strongly correlated with geographical distance. Genetic variation within each species are best explained by distinct spatial and environmental variables. SNP genotyping coupled with genotype-environment association analysis and phenotypic characterization of growth rate, suggested that the coexistence of three MPB fungal symbionts is the result of niche partitioning. We observed that both common (temperature seasonality and host species) and distinct (drought/cold stress, precipitation) environmental and spatial factors shaped these fungal genomes resulting in contrasting outcomes. Intraspecific phenotypic variations in <i>Gc </i>and <i>Ll</i> suggests potential for adaptive selection in these two species. By contrast, <i>Om</i> displayed narrower intraspecific variation but greater tolerance to high temperatures. Our study highlights the unique genotypic and phenotypic characteristics in these symbionts.</div>