The house mouse (Mus musculus), which is commensal to humans, has spread globally via human activities, leading to secondary contact between genetically divergent subspecies. This pattern of genetic admixture can provide insights into the selective forces at play in this well-studied model organism. Our analysis of 163 house mouse genomes, with a particular focus on East Asia, revealed substantial admixture between the subspeciescastaneusandmusculus, particularly in Japan and southern China. We revealed, despite the different level of autosomal admixture among regions, that all Y Chromosomes in the East Asian samples belonged to themusculus-type haplogroup, potentially explained by genomic conflict under sex-ratio distortion due to varying copy numbers of ampliconic genes on sex chromosomes,SlxandSly. Our computer simulations, designed to replicate the observed scenario, demonstrate that the preferential fixation ofmusculus-type Y Chromosomes can be achieved with a 10-20% increase in the male-to-female birth ratio. We also investigated the influence of selection on the post-hybridization of the subspeciescastaneusandmusculusin Japan. Even though the genetic background of most Japanese samples closely resembles the subspeciesmusculus, certain genomic regions overrepresented thecastaneus-like genetic components, particularly in immune-related genes. Furthermore, a large genomic block (~2 Mbp) containing a vomeronasal/olfactory receptor gene cluster predominantly harboredcastaneus-type haplotypes in the Japanese samples, highlighting the crucial role of olfaction-based recognition in shaping hybrid genomes.