We examined the effect of symbiont identity and heat stress on host metabolome and proteome in the cnidarian-dinoflagellate symbiosis. Exaiptasia diaphana (‘Aiptasia’) was inoculated with its native symbiont (Breviolum minutum) or a non-native symbiont (Symbiodinium microadriaticum; Durusdinium trenchii) and subjected to thermal stress. Host metabolomes were partially distinct at control temperature, however thermal stress caused profiles of anemones containing the two non-native symbionts to become more similar to each other and more distinct from those containing B. minutum. This may reflect symbiont densities; under control conditions, D. trenchii attained 60% and S. microadriaticum 15% of the density attained by B. minutum. At elevated temperature, only D. trenchii-colonised anemones experienced bleaching (60% loss). Combined metabolome and proteome analyses revealed the compounds that make up the thermal response of each symbiosis, either reflecting innate symbiont-specific differences or host-symbiont interactions. We show clear evidence of enhanced nutritional deprivation and cellular stress in hosts harbouring a novel symbiont following temperature stress, independent of the symbiont’s putative thermal resilience. Our findings highlight the physiological limits of partner switching as a means of adaptation to increased temperatures. However, we also offer preliminary evidence suggesting that metabolic functioning of the D. trenchii-Aiptasia association improves over the long-term.