Fusarium head blight (FHB) incited by Fusarium graminearum (Schw), is one of the most damaging diseases in wheat. FHB not only reduces grain yield drastically but also grain quality due to shriveled kernels and mycotoxin contamination. Host plant resistance is the most effective approach to combat the disease. To identify native quantitative trait loci (QTLs) from locally adapted cultivars, a population of 181 recombinant inbred lines (RILs) from Overland × Everest was genotyped using single nucleotide polymorphism (SNP) markers derived from genotyping-by-sequencing and phenotyped for fungal spread within the spike (type II), mycotoxin accumulation in grains (type III) and kernel damage (FDK) (type IV) in repeated greenhouse and field experiments. Six QTLs on chromosome regions of 1BL, 4A, 4BS, 5AL, 6BL and 7AS confers type II resistance with the resistance QTL on 1BL, 4BS, 6BL and 7AS from Everest and on 4A, 4BS and 5AL from Overland. The QTL on chromosome 4BS is overlapped with the reduced height gene Rht-B1. QTLs for type III and type IV resistance were mapped on chromosome 4BS, 5AL and 7AS and they overlapped with type II resistance in the same genomic regions. The haplotype analysis showed that genotypes containing multiple QTLs showed significantly higher resistance than those with fewer or no QTLs, indicating that minor QTLs from both parents had additive effects on FHB resistance. SNP markers tightly linked with QTLs were successfully converted into Kbiosciene kompetitive allelic specific PCR (KASP) assays that could be used in marker-assisted breeding for FHB resistance in wheat.