In order to reconcile existing data and hypotheses on the relationship outcomes of Caribbean Zoanthidea-Demospongiae symbioses, the context-dependent survival and growth (metrics of host sponge condition) were monitored for 8–12 months, with and without Zoanthidean symbionts, in native (coral reef) and novel (mangrove) habitats. Experiments repeated over space and time revealed significant positive effects of Zoanthidea colonization on metrics of host condition and indicated that the outcome of these symbioses can shift from mutualism to parasitism when transplanted to novel habitats. Although the precise mechanisms of the symbioses remain obscured and most of the species associations have not been examined, these experiments demonstrate an example where relationship outcomes are more conserved across their evolutionary history than host associations.