The lack of genomes from intermediate species between the Mus musculus and the rat has hindered the study of genomic mechanisms involved in the divergence of the mouse from the other mammals. Here, we present the complete genome sequences of Mus caroli and Mus pahari which diverged 3 MYA and 6 MYA from Mus musculus. The genomes of these two species enable an analysis of evolutionary dynamics within the Muridae lineage that uncovers the mechanisms which fashioned the specificity of the mouse genome. For instance, our analysis shows both that a wave of inter-chromosomal rearrangement occurring between 3 and 6 MYA shaped the karyotype of the laboratory mouse ancestor and that genome integration of retrogenes has been increased in the Mus lineage. By taking advantage of the comparable divergence time of Mus caroli and Mus pahari from the laboratory mouse with chimp and gorilla from human, we can unravel the evolutionary mechanisms specific to Muridae from evolutionary mechanisms common to both mammalian clades to better understand the evolutionary mechanisms that shaped the mouse genome.