Reef-building corals rely on photosynthate from endosymbiotic dinoflagellates (Symbiodiniaceae) to build the planet’s most biodiverse marine habitats. Unfortunately, environmental stress causes corals to lose these critical symbionts and risk starvation in a process called coral bleaching. Anthropogenic climate change has increased the frequency and severity of marine heat waves, leading to mass bleaching events and coral mortality. Because the coral animal is both mutualistic partner and habitat to the symbionts they host, host cellular conditions shape Symbiodiniaceae ecological dynamics. Therefore, predicting symbiotic stability under worsening climate change requires understanding how host cellular homeostasis responds to abiotic disturbance. This thesis tested the hypothesis that host cellular acid-base regulation is a thermosensitive juncture in the cnidarian-dinoflagellate symbiosis. I performed subacute heat challenges followed by broad assessments of symbiont and host cell and organismal physiology in three ecologically distinct symbiotic cnidarians: the reef-building coral Montipora capitata, the facultatively symbiotic model sea anemone Exaiptasia diaphana, and the facultatively symbiotic temperate coral Astrangia poculata. In M. capitata, heat stress acidified host intracellular pH (pHi) and led coral symbionts to retain photosynthate, decoupling partner recovery outcomes such that symbiont populations regrew before hosts recovered to pre-stress growth rates. Moreover, hosts receiving less symbiont photosynthate had lower pHi. Heat treatment also acidified pHi in both symbiotic and aposymbiotic E. pallida, but pHi was not affected by symbiont density or photosynthate translocation to the anemone host. In contrast, heat-treated A. poculata maintained similar pHi to controls and calcified more over the experiment, despite disintegration of symbiont cells and host tissue. Thus, heating disrupts pH homeostasis prior to symbiotic dysfunction in tropical cnidarians, but not in a temperate coral. I hypothesize that prior exposure to seasonal temperature fluctuations increases temperate coral pHi thermal resilience. Moreover, symbiotic dysfunction was only correlated with pHi acidification in an obligately symbiotic coral, and not in the two facultatively symbiotic cnidarians. Taken together, these results show that ocean warming directly impairs cnidarian pH regulation and suggest that the severity of this effect depends on cnidarians’ symbiotic needs and thermal histories. Thermal pHi dysregulation might contribute to symbiotic breakdown under climate change.