Hosting different symbiont species can affect inter-partner nutritional fluxes within the cnidarian-dinoflagellate symbiosis. Using nanoscale secondary ion mass spectrometry (NanoSIMS), we measured the spatial incorporation of photosynthetically fixed(13)C and heterotrophically derived(15)N into host and symbiont cells of the model symbiotic cnidarian Aiptasia (Exaiptasia pallida) when colonized with its native symbiontBreviolum minutumor the non-nativeDurusdinium trenchii.Breviolum minutumexhibited high photosynthetic carbon assimilationpercell and translocation to host tissue throughout symbiosis establishment, whereasD. trenchiiassimilated significantly less carbon, but obtained more host nitrogen. These findings suggest thatD. trenchiihas less potential to provide photosynthetically fixed carbon to the host despite obtaining considerable amounts of heterotrophically derived nitrogen. These sub-cellular events help explain previous observations that demonstrate differential effects ofD. trenchiicompared toB. minutumon the host transcriptome, proteome, metabolome and host growth and asexual reproduction. Together, these differential effects suggest that the non-native host-symbiont pairing is sub-optimal with respect to the host's nutritional benefits under normal environmental conditions. This contributes to our understanding of the ways in which metabolic integration impacts the benefits of a symbiotic association, and the potential evolution of novel host-symbiont pairings.