Microsatellites are short, repetitive DNA sequences that can rapidly expand and contract due to slippage during DNA replication. Despite their impacts on transcription, genome structure, and disease, relatively little is known about the evolutionary dynamics of these short sequences across long evolutionary periods. To address this gap in our knowledge, we performed comparative analyses of 304 available insect genomes. We investigated the impact of sequence assembly methods and assembly quality on the inference of microsatellite content, and we explored the influence of chromosome type and number on the tempo and mode of microsatellite evolution across one of the most speciose clades on the planet. Diploid chromosome number had no impact on the rate of microsatellite evolution or the amount of microsatellite content in genomes. We found that centromere type (holocentric or monocentric) is not associated with a difference in the amount of microsatellite content; however, in those species with monocentric chromosomes, microsatellite content tends to evolve faster than in species with holocentric chromosomes.