Stochastic population processes may cause differences between species histories and gene histories. These processes are assumed to only influence the most recent divergences in the tree of life; however, there may be underappreciated potential for microevolutionary processes to impact deep divergences. I used multispecies coalescent models to determine the impact of stochastic processes on deep phylogenomic histories. Here I show phylogenomic discordance between gene histories and species histories is expected at deep divergences for many eukaryotic taxa, and the probability of discordance increases with population size, generation time, and the number of species in the tree. Five eukaryotic clades (angiosperms, birds, harpaline beetles, mammals, and nymphalid butterflies) demonstrate significant discordance potential at divergences over 50 million years old, and this discordance potential is independent of the age of divergence. These findings demonstrate population processes acting over very short timescales will leave a lasting impact on genomic histories, even for divergence events occurring tens to hundreds of millions of years ago.