Significance Opportunities to study microevolution in wild populations are rare and challenging. Annual monitoring allowed us to capture both the prelude to and aftermath of one of the largest marine mass mortality events on record in a keystone marine species. Median mortality of 81% across populations was recorded along with significant allele frequency shifts at multiple loci in the adult population. Shifts were consistent across locations and also occurred in new recruits, with few exceptions. These results indicate a long-term species-wide change in allele frequencies will persist through future generations. Population genomic monitoring, at a time when marine diseases and mass mortalities are on the rise, will be essential for documenting rapid genetic shifts in response to chronic and extreme events.