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Abstract In contrast to the typified view of genome cycling only between haploidy and diploidy, there is evidence from across the tree of life of genome dynamics that alter both copy number (i.e. ploidy) and chromosome complements. Here, we highlight examples of such processes, including endoreplication, aneuploidy, inheritance of extrachromosomal DNA, and chromatin extrusion. Synthesizing data on eukaryotic genome dynamics in diverse extant lineages suggests the possibility that such processes were present before the last eukaryotic common ancestor. While present in some prokaryotes, these features appear exaggerated in eukaryotes where they are regulated by eukaryote-specific innovations including the nucleus, complex cytoskeleton, and synaptonemal complex. Based on these observations, we propose a model by which genome conflict drove the transformation of genomes during eukaryogenesis: from the origin of eukaryotes (i.e. first eukaryotic common ancestor) through the evolution of last eukaryotic common ancestor.