High-quality genome information is essential for efficiently deciphering and improving crop traits. Here, we report a highly contiguous and accurate hexaploid genome assembly for the key wheat breeding parent Zhou8425B, an elite 1BL/1RS translocation line with durable adult plant resistance (APR) against yellow rust (YR) disease. By integrating HiFi and Hi-C sequencing reads, we have generated a 14.75-Gb genome assembly for Zhou8425B with a contig N50 of 70.94 and a scaffold N50 of 735.11 Mb. Comparisons with previously sequenced common wheat cultivars shed light on structural changes in the 1RS chromosome arm, which has been extensively used in wheat improvement. Interestingly, Zhou8425B 1RS carries more genes encoding AP2/ERF-ERF or B3 transcription factors than its counterparts in four previously sequenced wheat and rye genotypes. The Zhou8425B genome assembly aided in the fine mapping of a new APR locus (YrZH3BS) that confers resistance to YR disease and promotes grain yield under field conditions. Notably, pyramiding YrZH3BS with two previously characterized APR loci (YrZH22 and YrZH84) can further reduce YR severity and enhance grain yield, with the triple combination (YrZH3B + YrZH22 + YrZH84) having the greatest effect. Finally, the founder genotype effects of Zhou8425B were explored using publicly available genome resequencing data, which reveals the presence of important Zhou8425B genomic blocks in its derivative cultivars. Our data demonstrate the value of the Zhou8425B genome assembly for further study of the structural and functional characteristics of 1RS, the genetic basis of durable YR resistance, and founder genotype effects in wheat breeding. Our resources will facilitate the development of elite wheat cultivars through genomics-assisted breeding.