In contrast to the typified view of genomes as fixed within species, we find considerable evidence for genome dynamics (e.g. cyclical polyploidization, chromosomal rearrangements) across the eukaryotic tree of life. Based on these data, we hypothesized that LECA, the last eukaryotic common ancestor, had a dynamic genome that used epigenetic mechanisms to distinguish germline (i.e. to be inherited) from somatic genome material. Though fewer data exist for bacteria and archaea, there is also evidence of genome dynamics among these lineages suggesting either multiple or very ancient origins of the dynamic processes. Together, these data challenge ideas on the nature of genomes across the tree of life.