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One approach to improve long-term coral restoration success utilizes naturally stress-tolerant corals from the wild. While the focus has primarily been on thermal stress, low oxygen is a growing threat to coral reefs and restoration efforts should also consider hypoxia tolerance. Here we determine if Siderastrea siderea and Agaricia tenuifolia populations from a reef with a historical record of low oxygen exhibit evidence of local adaptation to hypoxic events, compared to populations from a reference reef. We employed a laboratory-based reciprocal transplant experiment mimicking a severe 14-night hypoxic event and monitored bleaching responses, photo-physiology, metabolic rates, and survival of all four populations during, and for two weeks following the event. In both species, we found the populations from the hypoxic reef either fully persisted or recovered within 3 days of the event. In contrast, the conspecific naïve populations from the well-oxygenated reference reef experienced bleaching and death. This showcases the vulnerability of naïve corals exposed to low oxygen but also suggests that corals from the hypoxic reef locally adapted to survive severe episodic hypoxia. Other reefs with past episodic low oxygen may also be home to corals with adaptation signatures to hypoxia and may be useful for restoration efforts.