Knowledge on large-scale biological processes in the southern Red Sea is relatively limited, primarily due to the scarce in situ, and satellite-derived chlorophyll-a (Chl-a) datasets. During summer, adverse atmospheric conditions in the southern Red Sea (haze and clouds) have long severely limited the retrieval of satellite ocean colour observations. Recently, a new merged ocean colour product developed by the European Space Agency (ESA)—the Ocean Color Climate Change Initiative (OC-CCI)—has substantially improved the southern Red Sea coverage of Chl-a, allowing the discovery of unexpected intense summer blooms. Here we provide the first detailed description of their spatiotemporal distribution and report the mechanisms regulating them. During summer, the monsoon-driven wind reversal modifies the circulation dynamics at the Bab-el-Mandeb strait, leading to a subsurface influx of colder, fresher, nutrient-rich water from the Indian Ocean. Using satellite observations, model simulation outputs, and in situ datasets, we track the pathway of this intrusion into the extensive shallow areas and coral reef complexes along the basin’s shores. We also provide statistical evidence that the subsurface intrusion plays a key role in the development of the southern Red Sea phytoplankton blooms.