Marine heatwaves (MHWs) significantly disrupt marine ecosystems, affecting both macroflora and fauna. However, the impact on microorganisms is less understood despite temperature being a major determinant of microbial assemblage structure. Using data from thousands of Southern Hemisphere samples, the authors reveal that during the 2015/16 Tasman Sea MHW, temperatures approached or surpassed the upper thermal boundaries of many endemic taxa. Temperate microbial assemblages underwent a profound transition to niche states aligned with sites over 1000 km equatorward, adapting to higher temperatures and lower nutrient conditions brought about by the MHW. MHW conditions also modulate seasonal patterns of microbial diversity and support novel assemblage compositions. The most significant effects on microbial assemblages occurred during warmer months when temperatures exceeded the upper climatological bounds. Trends in microbial response across several MHWs in different locations suggest these are emergent properties of temperate ocean warming, which may facilitate monitoring, prediction, and adaptation efforts. The study highlights the importance of understanding microbial responses to extreme events for effective ecosystem management and conservation.Marine heatwaves (MHWs) significantly disrupt marine ecosystems, affecting both macroflora and fauna. However, the impact on microorganisms is less understood despite temperature being a major determinant of microbial assemblage structure. Using data from thousands of Southern Hemisphere samples, the authors reveal that during the 2015/16 Tasman Sea MHW, temperatures approached or surpassed the upper thermal boundaries of many endemic taxa. Temperate microbial assemblages underwent a profound transition to niche states aligned with sites over 1000 km equatorward, adapting to higher temperatures and lower nutrient conditions brought about by the MHW. MHW conditions also modulate seasonal patterns of microbial diversity and support novel assemblage compositions. The most significant effects on microbial assemblages occurred during warmer months when temperatures exceeded the upper climatological bounds. Trends in microbial response across several MHWs in different locations suggest these are emergent properties of temperate ocean warming, which may facilitate monitoring, prediction, and adaptation efforts. The study highlights the importance of understanding microbial responses to extreme events for effective ecosystem management and conservation.