Stripe rust (yellow rust) is a serious disease of bread wheat (Triticum aestivum L.) worldwide. Genetic resistance is considered the most economical, effective and environmentally friendly method to control the disease and to minimize the use of fungicides. The current study focused on characterizing the components of stripe rust resistance and understanding the interactions in Changwu 357-9 (CW357-9)/Avocet S RIL population. A genetic linkage map constructed using a new GenoBaits Wheat 16K Panel and the 660K SNP array had 5,104 polymorphic SNP markers spanning 3,533.11 cM. Four stable QTLs were detected on chromosome arms 1BL, 2AL, 3DS, and 6BS across all environments in Chngwu357-9. The most effective QTL QYrCW357-1BL was Yr29. The 6BS QTL was identified as Yr78, which has been combined with the 1BL QTL in many wheat cultivars and breeding lines. The novel QTL on 2AL with moderate effect showed a stable, significant epistatic interaction with Yr29. The QTL on 3DL should be same as QYrsn.nwafu-3DL and enriches the overall stripe rust resistance gene pool for breeding. Polymorphisms of flanking AQP markers AX-110020417 (for QYrCW357-1BL), AX-110020417 (for QYrCW357-2AL), AX-109466386 (for QYrCW357-3DL), and AX-109995005 (for QYrCW357-6BS), were evaluated in a diversity panel including 225 wheat cultivars and breeding lines. The results suggested that these high-throughput markers could be used to introduce QYrCW357-1BL (Yr29), QYrCW357-2AL, QYrCW357-3DL, and QYrCW357-6BS into commercial wheat cultivars. Combinations of these genes with other APR QTL should lead to higher levels of stripe rust resistance along with the beneficial effects of multi-disease resistance gene Yr29 on improving resistance to other diseases.