Microsatellites are widely used in population genetics, but their evolutionary dynamics remain poorly understood. It is unclear whether microsatellite loci drift in length over time. This is important because the mutation processes that underlie these important genetic markers are central to the evolutionary models that employ microsatellites. We identify more than 27 million microsatellites using a novel and unique dataset of modern and ancient Adélie penguin genomes along with data from 63 published chordate genomes. We investigate microsatellite evolutionary dynamics over two time scales: one based on Adélie penguin samples dating to approximately 46.5 kya, the other dating to the diversification of chordates more than 500 Mya. We show that the process of microsatellite allele length evolution is at dynamic equilibrium; while there is length polymorphism among individuals, the length distribution for a given locus remains stable. Many microsatellites persist over very long time scales, particularly in exons and regulatory sequences. These often retain length variability, suggesting that they may play a role in maintaining phenotypic variation within populations.