Understanding the drivers of evolutionary innovations provide a crucial perspective of how evolutionary processes unfold across taxa and ecological systems. In the Southern Ocean, the drivers of innovations are challenging to pinpoint as the evolutionary genetics of benthic fauna are influenced by signatures of Quaternary glacial-interglacial cycles, oceanic currents and species ecology. Here we examined the genome-wide single nucleotide polymorphisms of the Southern Ocean brittle stars Ophionotus victoriae (five arms, broadcaster) and O. hexactis (six arms, brooder). We found that O. victoriae and O. hexactis diverged at ~0.43 million years ago with interspecific gene flow. The species divergence time coincides with the timing of significant Antarctic Ice Sheet retreat (Marine Isotope Stage [MIS] 11). Within O. victoriae, contemporary gene flow can be linked to the Antarctic Circumpolar Current, and regional and local oceanographic regimes. Gene flow connecting West and East Antarctic islands near the Polar Front was also detected in O. hexactis. The evolutionary innovations in O. hexactis (increase in arm number and switch to brooding from broadcasting) were linked to selection under intense deglacial meltwater during MIS 11. We highlight intense interglacial-glacial cycles in the recent past can lead to innovative evolutionary changes and species divergence.