The genomes of organisms living in diverse environments can reflect adaptations to diverse environmental conditions. Anthropogenic disturbances such as soil pollution can quickly create steep environmental gradients that likely induce adaptation and imprint genomic signatures of selection. Fungi are ubiquitous in soil environments and are key players in soil systems processes, however little is known about how they evolve in face of anthropogenic soil pollution. We used population genomics to investigate incipient local adaptation to heavy metals in Suillus luteus, a widespread symbiotic ectomycorrhizal fungus associated with pine trees. Available phenotypic data show that S. luteusisolates from the same population have variable heavy metal tolerance with some isolates tolerating high metal concentrations, while others show reduced growth and death when exposed to heavy metals. Whole genome scans across isolates from both habitats revealed genomic signatures associated with colonizing polluted sites, with a strong enrichment for transmembrane transporters. Candidate genes underlying heavy metal adaptation in S. luteus were involved in metal exclusion, immobilization, and detoxification, and displayed both allelic and copy number variation. Results from our study revealed incipient local adaptation to heavy metals in S. luteusand elucidate on the evolutionary processes involved in environmental adaptation in fungi.