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Abstract A species tree is a central concept in evolutionary biology whereby a single branching phylogeny reflects relationships among species. However, the phylogenies of different genomic regions often differ from the species tree. Although tree discordance is widespread in phylogenomic studies, we still lack a clear understanding of how variation in phylogenetic patterns is shaped by genome biology or the extent to which discordance may compromise comparative studies. We characterized patterns of phylogenomic discordance across the murine rodents—a large and ecologically diverse group that gave rise to the laboratory mouse and rat model systems. Combining recently published linked-read genome assemblies for seven murine species with other available rodent genomes, we first used ultraconserved elements (UCEs) to infer a robust time-calibrated species tree. We then used whole genomes to examine finer-scale patterns of discordance across ∼12 million years of divergence. We found that proximate chromosomal regions tended to have more similar phylogenetic histories. There was no clear relationship between local tree similarity and recombination rates in house mice, but we did observe a correlation between recombination rates and average similarity to the species tree. We also detected a strong influence of linked selection whereby purifying selection at UCEs led to appreciably less discordance. Finally, we show that assuming a single species tree can result in substantial deviation from the results with gene trees when testing for positive selection under different models. Collectively, our results highlight the complex relationship between phylogenetic inference and genome biology and underscore how failure to account for this complexity can mislead comparative genomic studies.