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Filamentous fungi rapidly evolve in response to environmental selection pressures in part due to their genomic plasticity. Parastagonospora nodorum, a fungal pathogen of wheat and causal agent of septoria nodorum blotch, responds to selection pressure exerted by its host, influencing the gain, loss, or functional diversification of virulence determinants, known as effector genes. Whole genome resequencing of 197 P. nodorum isolates collected from spring, durum, and winter wheat production regions of the United States enabled the examination of effector diversity and genomic regions under selection specific to geographically discrete populations. 1,026,859 SNPs/InDels were used to identify novel loci, as well as SnToxA and SnTox3 as factors in disease. Genes displaying presence/absence variation, predicted effector genes, and genes localized on an accessory chromosome had significantly higher pN/pS ratios, indicating a higher rate of sequence evolution. Population structure analyses indicated two P. nodorum populations corresponding to the Upper Midwest (Population 1) and Southern/Eastern United States (Population 2). Prevalence of SnToxA varied greatly between the two populations which correlated with presence of the host sensitivity gene Tsn1 in the most prevalent cultivars in the corresponding regions. Additionally, 12 and 5 candidate effector genes were observed to be under diversifying selection among isolates from Population 1 and 2, respectively, but under purifying selection or neutrally evolving in the opposite population. Selective sweep analysis revealed 10 and 19 regions that had recently undergone positive selection in Population 1 and 2, respectively, involving 92 genes in total. When comparing genes with and without presence/absence variation, those genes exhibiting this variation were significantly closer to transposable elements. Taken together, these results indicate that P. nodorum is rapidly adapting to distinct selection pressures unique to spring and winter wheat production regions by rapid adaptive evolution and various routes of genomic diversification, potentially facilitated through transposable element activity. Parastagonospora nodorum is an economically important pathogen of wheat, employing proteinaceous effectors to cause disease. Recognition of effectors by host susceptibility genes often leads to the elicitation of programmed cell death. However, little is known on the correlation between effector diversity and the spatial distribution of host resistance/susceptibility or the genomic mechanisms of diversification. This research presents the genome resequencing of 197 P. nodorum isolates collected from spring, winter, and durum wheat production regions of the United States, enabling the investigation of genome dynamics and evolution. Results illustrate local adaptation to host resistance or susceptibility, as evidenced by population-specific evolution of predicted effector genes and positively selected selective sweeps. Predicted effector genes, genes exhibiting presence/absence variation, and genes residing on an accessory chromosome, were found to be diversifying more rapidly. Additionally, transposable elements were predicted to play a role in the maintenance or elimination of genes. A GWAS approach identified the previously reported SnToxA and SnTox3 as well as novel virulence candidates as major elicitors of disease. These results highlight the flexibility of the P. nodorum genome in response to population-specific selection pressures and illustrate the utility of whole genome resequencing for the identification of putative virulence mechanisms. [ABSTRACT FROM AUTHOR]