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Background: Fusarium head blight resistance genes, Fhb1 (for Type-II resistance), Fhb2 (Type-II), and Fhb5 (Type-I plus some Type-II), which originate from Sumai 3, are among the most important that confer resistance in hexaploid wheat. Near-isogenic lines (NILs), in the CDC Alsask (susceptible; n = 32) and CDC Go (moderately susceptible; n = 38) backgrounds, carrying these genes in all possible combinations were developed using flanking microsatellite markers and evaluated for their response to FHB and deoxynivalenol (DON) accumulation in eight environments. NILs were haplotyped with wheat 90 K iSelect assay to elucidate the genomic composition and confirm alleles' presence. Other than evaluating the effects of three major genes in common genetic background, the study elucidated the epistatic gene interactions as they influence FHB measurements; identified loci other than Fhb1, Fhb2, and Fhb5, in both recurrent and donor parents and examined annotated proteins in gene intervals., Results: Genotyping using 81,857 single nucleotide polymorphism (SNP) markers revealed polymorphism on all chromosomes and that the NILs carried < 3% of alleles from the resistant donor. Significant improvement in field resistance (Type-I + Type-II) resulted only among the CDC Alsask NILs, not the CDC Go NILs. The phenotypic response of NILs carrying combinations of Sumai 3 derived genes suggested non-additive responses and Fhb5 was as good as Fhb1 in conferring field resistance in both populations. In addition to Fhb1, Fhb2, and Fhb5, four to five resistance improving alleles in both populations were identified and three of five in CDC Go were contributed by the susceptible parent. The introgressed chromosome regions carried genes encoding disease resistance proteins, protein kinases, nucleotide-binding and leucine rich repeats' domains. Complex epistatic gene-gene interactions among marker loci (including Fhb1, Fhb2, Fhb5) explained > 20% of the phenotypic variation in FHB measurements., Conclusions: Immediate Sumai 3 derivatives carry a number of resistance improving minor effect alleles, other than Fhb1, Fhb2, Fhb5. Results verified that marker-assisted selection is possible for the introgression of exotic FHB resistance genes, however, the genetic background of the recipient line and epistatic interactions can have a strong influence on expression and penetrance of any given gene.