We compared existing Porites data with bleached and unbleached colonies of the branching coral P. compressa collected in Kaneohe Bay Hawaii during the 2015 coral bleaching event. Loci that mapped to coral, symbiont, and microbial references revealed genetic structure consistent with recent host-symbiont co-evolution. Cryptic genetic clades were resolved that previous work has associated with distance from shore, but no genetic structure was associated with bleaching. We identified many candidate loci associated with morphospecies, including candidate host and symbiont loci with fixed differences between branching and mounding corals. We also found many loci associated with cryptic genetic structure, yet relatively few loci associated with bleaching. Recent host-symbiont co-evolution and rapid diversification suggests that variation and therefore the capacity of these corals to adapt may be underappreciated.