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Wheat curl mite (Aceria tosichella Keifer) is an important wheat (Triticum aestivum L. em. Thell.) pest in many wheat‐growing regions worldwide. Mite feeding damage not only directly affects wheat yield, but A. tosichella also transmits Wheat streak mosaic virus (WSMV). Wheat resistance to A. tosichella, therefore, helps control WSMV. OK05312 (PI 670019) is an advanced breeding line released from Oklahoma that shows a high level of A. tosichella resistance. To map the gene(s) conditioning wheat resistance to A. tosichella in OK05312, a genetic linkage map was constructed using single nucleotide polymorphism (SNP) markers derived from genotyping‐by‐sequencing (GBS) and a population of 186 recombinant inbred lines (RILs) from the cross 'Jerry' (PI 632433)/OK05312. Seedlings of both parents and the RIL population were infested by A. tosichella Biotype 1 in greenhouse experiments. One major quantitative trait locus was identified on the short arm of chromosome 6D, which corresponds to the previously reported gene Cmc4 for A. tosichella resistance. This gene explained up to 71% of the phenotypic variation and was delimited in a 1.7‐Mb (∼3.3‐cM) region by SNPs 370SNP7523 and 370SNP1639. We successfully converted 12 GBS‐SNPs into Kompetitive allele specific polymerase chain reaction (KASP) markers. Two of them tightly linked to Cmc4 were validated to be highly diagnostic in a US winter wheat population and can be used for marker‐assisted breeding for incorporation of Cmc4 into new wheat cultivars. [ABSTRACT FROM AUTHOR]