The genomic basis of cladogenesis and adaptive evolutionary change has intrigued biologists for decades. The unique insights gained from a genome-level perspective have revealed a striking pattern of conserved macrosynteny within chromosomes across huge phylogenetic distances in animals, yet progress in many lineages has been hampered by the absence of genome-level data. Here, we show that the tectonics of genome evolution in clitellates, a clade composed of most freshwater and all terrestrial species of the phylum Annelida, is characterised by extensive genome-wide scrambling that resulted in a massive loss of macrosynteny between marine annelids and clitellates, to the point that ancient bilaterian linkage groups (ie, groups of genes inherited as a block in most bilaterian phyla) are fully disrupted. These massive rearrangements included the formation of putative neocentromeres with newly acquired transposable elements, and preceded a further period of genome-wide reshaping events including whole-genome duplications and massive macrosyntenic reshuffling between clitellate lineages, potentially triggered by the loss of genes involved in genome stability and homeostasis of cell division. Notably, while these rearrangements broke short-range interactions observed between Hox genes in marine annelids, they were reformed as long-range interactions in clitellates. These genomic rearrangements led to the relocation of genes and the formation of new chimeric genetic elements, both of which may have contributed to the adaptation of clitellates to freshwater and terrestrial environments. Our findings reveal extensive genomic reshaping in clitellates at both the linear (2D) and three-dimensional (3D) levels, suggesting that, unlike in other animal lineages where synteny conservation constraints structural evolution, clitellates exhibit a remarkable tolerance for chromosomal rearrangements. Our study thus suggests that the genomic landscape of Clitellata resulted from a rare burst of genomic changes that ended a long period of stability that persists across large phylogenetic distances.