Chromosomal fusions have been hypothesized to facilitate evolutionary adaptation, but empirical evidence has been scarce. We examined patterns of genome evolution in the copepod Eurytemora affinis species complex, which are numerically dominant and highly invasive, with the extraordinary capacity to rapidly invade novel salinities. Prior studies from my laboratory (Lee Lab) revealed parallel selection acting on the same sets of ion transporter genes during independent saline to freshwater invasions by populations from genetically distinct clades. Our chromosome-level genomes of three genetically divergent clades of this species complex revealed peculiar genome architectures that might contribute to their remarkable capacity to acclimate and evolve during salinity invasions. Among the three genetically distinct clades of E. affinis complex, we discovered independent chromosomal fusions in two different clades, with the Europe clade (E. affinis proper) having 15 chromosomes, fusing independently into 7 chromosomes in the Gulf clade (E. gulfia) and 4 chromosomes in the Atlantic clade (E. carolleeae). Notably, for the highly invasive Atlantic clade (E. carolleeae), chromosomal fusion sites, especially the centromeres, were significantly enriched with signatures of selection associated with contemporary shifts from saline to freshwater habitats. These chromosomal fusions joined functionally-related ion transporter genes, forming "supergenes" at the centromeres, where recombination is low. This study uncovers novel patterns of genome architecture evolution with potentially important implications for mechanisms of adaptive evolution in response to radical environmental change.