Bitterling fishes, which is Cyprinid of the subfamily Acheilognathinae, exhibit a unique reproductive ecology, in that they lay their eggs inside the gills of living Unionidae mussels. This has been hypothesized to result in a remarkable diversity of egg shapes within this group and to contribute to species diversification, although the developmental, molecular, and evolutionary mechanisms behind these changes remain elusive. This study utilized Acheilognathus bitterling fishes, which exhibits parallel evolution of elliptical egg shape among closely related species, to observe egg shape changes and explore potential factors in vitro, and estimate evolutionary history through phylogenetic analysis based on whole-genome data. A. tabira species, subspecies producing long elliptical eggs showed elongation of short elliptical oocytes during the final maturation stage with nuclear migration. In contrast, subspecies producing short elliptical eggs showed similar initial elongation during the maturation, but reverted to their original shape after nuclear envelope breakdown. Conversely, in species other than A. tabira that produce long elliptical eggs, elongation was already observed at the end of the growth phase. These eggs underwent further elongation during the final maturation stage, as observed in A. tabira, but reverted to their original long elliptical shape following nuclear envelope breakdown. Inhibition assays of cytoskeletal factors revealed that actin filament polymerization caused rapid reversion of elongated oocytes to short elliptical shapes in all species. However, this did not occur in mature eggs with developed egg membranes. Phylogenetic analysis revealed extensive hybridization within the genus. These results suggest that the evolution of egg shape in this genus is due to differences in the stability of egg shape, which elongates in an actin-dependent manner during the growth phase to the final maturation stage, and the fixation of egg morphology with egg membrane development, possibly facilitated by hybridization.