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While population genomic analyses based on reference genome alignments offer valuable insights into how gene variants are distributed across populations, these approaches fail to capture intraspecific variation in genes absent from the reference genome. Pan-genomic analyses based on de novo assemblies offer a promising alternative to reference-based genomics with the potential to address the full genetic repertoire of a species. Here, we evaluate 260 genome sequences of<jats:italic>A<\/jats:italic>.<jats:italic>fumigatus<\/jats:italic>including 62 newly sequenced strains, using a combination of population genomics, phylogenomics, and pan-genomics. Our results offer a high-resolution assessment of population structure and recombination frequency, phylogenetically structured gene presence\u2013absence variation, evidence for metabolic specificity, and the distribution of putative antifungal resistance genes. Although<jats:italic>A<\/jats:italic>.<jats:italic>fumigatus<\/jats:italic>disperses primarily via asexual conidia, we identified extraordinarily high levels of recombination with the lowest linkage disequilibrium decay value reported for any fungal species to date. We provide evidence for 3 primary populations of<jats:italic>A<\/jats:italic>.<jats:italic>fumigatus<\/jats:italic>, with recombination occurring only rarely between populations and often within them. These 3 populations are structured by both gene variation and distinct patterns of gene presence\u2013absence with unique suites of accessory genes present exclusively in each clade. Accessory genes displayed functional enrichment for nitrogen and carbohydrate metabolism suggesting that populations may be stratified by environmental niche specialization. Similarly, the distribution of antifungal resistance genes and resistance alleles were often structured by phylogeny. Altogether, the pan-genome of<jats:italic>A<\/jats:italic>.<jats:italic>fumigatus<\/jats:italic>represents one of the largest fungal pan-genomes reported to date including many genes unrepresented in the Af293 reference genome. These results highlight the inadequacy of relying on a single-reference genome-based approach for evaluating intraspecific variation and the power of combined genomic approaches to elucidate population structure, genetic diversity, and putative ecological drivers of clinically relevant fungi.<\/jats:p>","DOI":"10.1371\/journal.pbio.3001890","type":"journal-article","created":{"date-parts":[[2022,11,17]],"date-time":"2022-11-17T19:17:31Z","timestamp":1668712651000},"page":"e3001890","update-policy":"https:\/\/doi.org\/10.1371\/journal.pbio.corrections_policy","source":"Crossref","is-referenced-by-count":90,"title":["The pan-genome of Aspergillus fumigatus provides a high-resolution view of its population structure revealing high levels of lineage-specific diversity driven by recombination"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0632-102X","authenticated-orcid":true,"given":"Lotus A.","family":"Lofgren","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brandon S.","family":"Ross","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert A.","family":"Cramer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jason E.","family":"Stajich","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2022,11,17]]},"reference":[{"key":"pbio.3001890.ref001","article-title":"Antibiotic Resistance Threats in the United States","author":"Centers for Disease Control and Prevention (U.S.)","year":"2019","journal-title":"US Department of Health and Human Services, Centers for Disease Control and Prevention."},{"key":"pbio.3001890.ref002","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1016\/j.mib.2005.06.017","article-title":"Aspergillus fumigatus: saprophyte or pathogen?","volume":"8","author":"F Tekaia","year":"2005","journal-title":"Curr Opin Microbiol"},{"key":"pbio.3001890.ref003","article-title":"Aspergillus fumigatus and Aspergillosis in 2019","volume":"201933","author":"J-P Latg\u00e9","journal-title":"Clin Microbiol Rev"},{"key":"pbio.3001890.ref004","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1016\/j.ijantimicag.2006.08.017","article-title":"Multi-azole resistance in Aspergillus fumigatus","volume":"28","author":"SJ Howard","year":"2006","journal-title":"Int J Antimicrob Agents"},{"key":"pbio.3001890.ref005","doi-asserted-by":"crossref","first-page":"2430","DOI":"10.1038\/s41564-019-0558-7","article-title":"Fungal biofilm morphology impacts hypoxia fitness and disease progression","volume":"4","author":"CH Kowalski","year":"2019","journal-title":"Nat Microbiol"},{"key":"pbio.3001890.ref006","doi-asserted-by":"crossref","first-page":"e00135","DOI":"10.1128\/mBio.00135-17","article-title":"Heterogeneity Confounds Establishment of \u201ca\u201d Model Microbial Strain","volume":"8","author":"N. 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