This study reported a quantitative trait locus (QTL) mapping for identifying the adult-stage powdery mildew resistance genes in a recombinant inbred line (RIL) population of common wheat (Triticum aestivum L.). This population was derived from the highly susceptible variety Ningchun 4 crossing with the highly resistant variety Ningchun 27, and genotyped using genotyping-by-sequencing (GBS) approach. The results showed that the additive-epistatic genetic model using four pairs of major genes was suitable for identifying the powdery mildew resistance loci. Two resistance-conferring loci QPm.naafs-4D and QPm.naafs-7D have been identified from Ningchun 27 and Ningchun 4, respectively. Out of them, QPm.naafs-4D represented a LOD value of 5.9 to 15.4 at multiple environmental conditions (additive effects: -1.1 to -1.2), and contributed to a phenotypic variation of 18.6% to 34.5%. This locus was delimited to a genetic distance of 4 cM harboring the durable poly-resistance gene Pm46/Lr67/Yr46/Sr55. Sequence analysis confirmed that QPm.naafs-4D in Ningchun 27 was identical to Pm46/Lr67/Yr46/Sr55. The resistance-conferring donor line is valuable in marker-assisted breeding for powdery mildew resistance in wheat.