Coral reefs face escalating pressures leading to unprecedented declines in the populations of reef-building corals.1,2 Conservation genomic studies are critical in understanding and formulating interventions to reverse such declines but thus far have only focused on a handful of broadcast-spawning species in shallow waters.3,4 The recent International Union for Conservation of Nature (IUCN) reclassification of six different brooding corals as "critically endangered"5 indicates that such species are equally threatened. However, we lack a thorough understanding of the factors underlying their decline. Here, we comprehensively examine the genetic impacts of a severe population decline in the brooding coral Helioseris cucullata, once a major contributor to Caribbean reefs but now critically endangered.6,7,8 Genome-wide sequencing of colonies across five locations revealed the presence of two distinct species, indicating that the remaining population sizes are even smaller than previously estimated. Using an exhaustive, spatially explicit sampling approach (across a total of ∼2.5 hectares), we observed extremely low genetic diversity and identified how localized dispersal, excessive inbreeding, and prevalent asexual reproduction may contribute to an extinction vortex. However, we also found evidence for recent hybridization and introgression, providing an avenue for the reintroduction of genetic diversity into both lineages. With many brooding species now under threat, these results highlight the critical need to assess the genetic processes associated with their declines so that these can be harnessed or mitigated to deliver effective conservation outcomes.