Elevated temperatures can produce a range of serious, deleterious effects on marine invertebrate—Symbiodinium symbioses. The responses of free-living Symbiodinium to elevated temperature, however, have been little studied, especially in the context of their natural habitat. In this study, we investigated physiological responses of two Symbiodinium cultures to elevated temperature, an exclusively free-living ITS2 clade A (strain HI-0509) and the symbiosis-forming ITS2 type A1 (strain CCMP2467). Free-living Symbiodinium strains have recently been isolated from benthic sediments, and both cultures were therefore grown with or without a microhabitat of carbonate sediment at 25, 28 or 31 °C. Maximum quantum yield of photosystem II (F v/F m) and specific growth rate were measured as response variables. In culture, Symbiodinium cells exhibit motility in a helical swimming pattern, and therefore, revolutions per minute (RPM) were also measured with video microscopy. The exclusively free-living clade A was physiologically superior to Symbiodinium A1 across all measured variables and treatment combinations. F v/F m remained relatively stable through time (at approximately 0.55) and was not substantially affected by temperature or the presence or the absence of sediment. Populations of the exclusively free-living Symbiodinium A reproduced faster with sediment than without and exhibited high levels of motility across all treatments (surpassing 300 RPM). In contrast, the F v/F m of A1 dropped to 0.42 in sediment (relative to cultures without sediment) and exhibited dramatic declines in cell concentration, most severely at 31 °C. A > 50 % reduction in motility was also observed at 31 °C. Even in the absence of sediment, elevated temperature was observed to reduce population growth and cell motility of type A1. We suggest that vital behaviours linked to motility (such as vertical migration and the locating of potential hosts) may become impaired during future thermal anomalies and that populations of Symbiodinium A1 may only live transiently in sediment or outside coral hosts. Such differences in physiology between distinct Symbiodinium types may represent adaptations that are either conserved or lost depending on the differing selection pressures that come with living in symbiosis or free in the environment.