Accurate estimates of species relationships are integral to our understanding of the evolution of traits and lineages, yet many relationships remain controversial despite whole genome sequence data. These controversies are due, at least in part, to complex patterns of phylogenetic and non-phylogenetic signal coming from regions of the genome experiencing different evolutionary forces. Here we profile the phylogenetic informativeness of loci from across mammalian genomes. We identified orthologous sequences from primates, rodents, and pecora, and annotated millions of sites as one or more of nine locus types (e.g. coding, intronic, intergenic) and profiled the informativeness of different locus types across the evolutionary timescales of each clade. In all cases, non-coding loci provided more overall signal and a higher proportion of phylogenetic signal compared to coding loci. Most locus types provide relatively consistent phylogenetic information across timescales, although we find evidence that coding and intronic regions may inform disproportionately about older and younger splits, respectively, to a limited degree. We also validated the SISRS pipeline as an annotation-free ortholog discovery pipeline that identifies millions of phylogenetically informative sites directly from whole-genome sequencing reads.