Genomic evolution is shaped by a dynamic combination of mutation, selection and genetic drift. These processes lead to evolutionary rate variation across loci and among lineages. In turn, interactions between these two forms of rate variation can produce residual effects, whereby the pattern of among-lineage rate heterogeneity varies across loci. The nature of rate variation is encapsulated in the pacemaker models of genome evolution, which differ in the degree of importance assigned to residual effects: none (Universal Pacemaker), some (Multiple Pacemaker) or total (Degenerate Multiple Pacemaker). Here we use a phylogenetic method to partition the rate variation across loci, allowing comparison of these pacemaker models. Our analysis of 431 genes from 29 mammalian taxa reveals that rate variation across these genes can be explained by 13 pacemakers, consistent with the Multiple Pacemaker model. We find no evidence that these pacemakers correspond to gene function. Our results have important consequences for understanding the factors driving genomic evolution and for molecular-clock analyses.