Reef-building corals depend upon a nutritional endosymbiosis with photosynthetic dinoflagellates of the family Symbiodiniaceae for the majority of their energetic needs. While this mutualistic relationship is impacted by numerous stressors, warming oceans are a predominant threat to coral reefs, placing the future of the world’s reefs in peril. Some Symbiodiniaceae species exhibit tolerance to thermal stress, but the in hospite symbiont response to thermal stress is underexplored. To describe the underpinnings of symbiosis and heat stress response, we compared in hospite and free-living transcriptomes of Durusdinium trenchii, a pan-tropical heat-tolerant Symbiodiniaceae species, under stable temperature conditions and acute hyperthermal stress. We discovered that symbiotic state was a larger driver of the transcriptional landscape than heat stress. The majority of differentially expressed transcripts between in hospite and free-living cells were downregulated, suggesting the in hospite condition is associated with the shutdown of numerous processes uniquely required for a free-living lifestyle. In the free-living state, we identified enrichment for numerous cell signaling pathways and other functions related to detecting and responding to a changing environment, as well as transcripts relating to mitosis, meiosis, and motility. In contrast, in hospite cells exhibited enhanced transcriptional activity for photosynthesis and carbohydrate transport as well as chromatin modifications and a disrupted circadian clock. Hyperthermal stress induced drastic alteration of transcriptional activity in hospite, suggesting symbiotic engagement with the host elicited an exacerbated stress response when compared to free-living D. trenchii. Altogether, the dramatic differences in gene expression between in hospite and free-living D. trenchii indicate the importance of considering symbiotic state in investigations of symbiosis and hyperthermal stress in Symbiodiniaceae.