The consideration of ‘mutual benefits’ and partner cooperation have long been the accepted standpoint from which to draw inference about the onset, maintenance and breakdown of the coral-algae endosymbiosis. In this paper, I review recent research into the climate-induced breakdown of this important symbiosis (namely ‘coral bleaching’) that challenges the validity of this long-standing belief. Indeed, I introduce a more parsimonious explanation, in which the coral host exerts a ‘controlled parasitism’ over its algal symbionts that is akin to an enforced domestication arrangement. Far from being pathogenic, a range of well-established cellular processes are reviewed that support the role of the coral host as an active ‘farmer’ of the energy-rich photoassimilates from its captive symbionts. Importantly, this new paradigm reposes the deleterious bleaching response in terms of an envelope of environmental conditions in which the exploitative and captive measures of the coral host are severely restricted. The ramification of this new paradigm for developing management strategies that may assist the evolution of bleaching resistance in corals is discussed.