Fusarium head blight (FHB) is a serious fungal disease of wheat (Triticum aestivum L.) that reduces both grain yield and quality with mycotoxins. Little is known about FHB disease and its causal agents in Georgia. The objectives of this research included: i) assessing recent FHB epidemics in Georgia, ii) exploring pathogen population structure and genetic diversity, and iii) identifying host resistance loci. Forty-four soft red winter wheat (SRWW) fields were assessed for disease during the 2018 and 2019 FHB outbreaks. The combination of hours of conducive temperature (T = 15 to 30 ºC) and higher relative humidity (RH ≥ 90%) post-anthesis best predicted FHB epidemics. A total of 196 Fusarium species were isolated from wheat and corn fields during 2018 and 2019. Phylogenetic analysis using the translation elongation factor 1-alpha and RNA polymerase second largest subunit gene sequence resolved isolates into 185 haplotypes, representing 12 Fusarium species grouped into five species complexes. F. graminearum with 15-acetyl-deoxynivalenol (15ADON) chemotype and F. incarnatum were the dominant species from wheat and corn, respectively, suggesting corn might not be serving as a pathogen reservoir for FHB. A total of 82 multilocus genotypes (MLGs) across 86 F. graminearum isolates were grouped into two clusters and our populations resembled a part of the larger North American population. Our results indicated that higher genetic diversity across F. graminearum could have been contributed by migration and local adaption; however, populations in Georgia were mostly clonal counterbalancing the diversity. A GWAS conducted on 236 elite SRWW lines identified eleven major-effect quantitative trait loci (QTLs) across five FHB traits. Three QTLs were stable and five exhibited a pleiotropic effect. QTLs QFhb-3BL, QFhb-5AS, QFhb-5BL, QFhb-7AS.1, QFhb-7AS.2, and QFhb-7BS are presumed to be novel. Pyramiding resistance alleles from major QTLs significantly reduced FHB parameters. In summary, this study has expanded the understanding of FHB epidemics and pathogen population dynamics in Georgia and identified potential resistance loci from the native wheat gene pool. This information will be invaluable to making an informed decision on implementing effective and integrated disease management strategies including host resistance to mitigate the future impacts of FHB on wheat.