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This study investigates the physiological response to heat stress of three genetically different Symbiodiniaceae strains isolated from the scleractinian coral Mussismilia braziliensis, endemic of the Abrolhos Bank, Brazil. Cultures of two Symbiodinium sp. and one Cladocopium sp. were exposed to a stepwise increase in temperature (2°C every second day) ranging from 26°C (modal temperature in Abrolhos) to 32°C (just above the maximum temperature registered in Abrolhos during the third global bleaching event—TGBE). After the cultures reached their final testing temperature, reactive oxygen species (ROS) production, single cell attributes (relative cell size and chlorophyll fluorescence), and photosynthetic efficiency (effective (Y(II)) and maximum (Fv/Fm) quantum yields) were measured within 4 h and 72 h. Non-photochemical coefficient (NPQ) was estimated based on fluorescence values. Population average ROS production was variable across strains and exposure times, reaching up a 2-fold increase at 32°C in one of the Symbiodinium sp. strains. A marked intrapopulation difference was observed in ROS production, with 5 to 25% of the cells producing up to 10 times more than the population average, highlighting the importance of single cell approaches to assess population physiology. Average cell size increases at higher temperatures, likely resulting from cell cycle arrest, whereas chlorophyll fluorescence decreased, especially in 4 h, indicating a photoacclimation response. The conditions tested do not seem to have elicited loss of photosynthetic efficiency nor the activation of non-photochemical mechanisms in the cells. Our results unveiled a generalized thermotolerance in three Symbiodiniaceae strains originated from Abrolhos’ corals. Inter and intra-specific variability could be detected, likely reflecting the genetic differences among the strains.