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Fusarium ear rot (FER), caused by the fungal pathogen Fusarium verticillioides, stands as one of the most economically burdensome and pervasive diseases affecting maize worldwide. Its impact on food security is particularly pronounced due to the production of fumonisins, toxic secondary metabolites that pose serious health risks, especially for livestock. FER disease severity is complex and polygenic, with few resistance (R) genes being identified for use in breeding resistant varieties. While FER is the subject of several breeding programs, only a few studies have investigated entire populations of F. verticillioides with corresponding virulence data to better understand and characterize the pathogenomics. Here, we sequenced and compared the genomes of 50 Fusarium isolates (43 F. verticillioides and 7 other Fusarium spp.) that were used to inoculate a diverse maize population. Our objectives were to elucidate the genome size and composition of F. verticillioides, explore the variable relationship between fumonisin production and visual disease severity, and shed light on the phylogenetic relationships among the isolates. Additionally, we conducted a comparative analysis of the nucleotide variants (SNPs) and the isolates' effectoromes to uncover potential genetic determinants of pathogenicity. Our findings revealed several promising leads, notably the association of certain gene groups, such as pectate lyase, with disease severity. These genes should be investigated further as putative alleles for breeding resistant maize varieties. We suggest that, beyond validation of the alleles identified in this study, researchers validate each phenotypic dataset on an individual basis, particularly if considering fumonisin concentrations and when using diverse populations. Our study underscores the importance of genomic analysis in tackling FER and offers insights that could inform the development of resilient maize cultivars. By leveraging advances in genomics and incorporating pathogen populations into breeding programs, resistance to FER can be advanced. [ABSTRACT FROM AUTHOR]