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Abstract Using recently published chromosome‐length genome assemblies of two damselfly species,Ischnura elegansandPlatycnemis pennipes, and two dragonfly species,Pantala flavescensandTanypteryx hageni, we demonstrate that the autosomes of Odonata have undergone few fission, fusion, or inversion events, despite 250 million years of separation. In the four genomes discussed here, our results show that all autosomes have a clear ortholog in the ancestral karyotype. Despite this clear chromosomal orthology, we demonstrate that different factors, including concentration of repeat dynamics, GC content, relative position on the chromosome, and the relative proportion of coding sequence all influence the density of syntenic blocks across chromosomes. However, these factors do not interact to influence synteny the same way in any two pairs of species, nor is any one factor retained in all four species. Furthermore, it was previously unknown whether the micro‐chromosomes in Odonata are descended from one ancestral chromosome. Despite structural rearrangements, our evidence suggests that the micro‐chromosomes in the sampled Odonata do indeed descend from an ancestral chromosome, and that the micro‐chromosome inP. flavescenswas lost through fusion with autosomes.