Large benthic foraminifera are an integral component of shallow-water tropical habitats and like many marine calcifiers are susceptible to ocean acidification (OA) and ocean warming (OW). In particular, the prolific Symbiodiniaceae-bearing and high-magnesium calcite Marginopora vertebralis has a low threshold compared to several diatom-bearing and low-magnesium calcite species. In this multi-year mesocosm experiment we tested three RPC 8.5 climate change scenarios (i) present day, (ii) the year 2050, and (iii) 2100. To enable a realistic epiphytic association these experiments were uniquely conducted using natural carbonate substrate, living calcifying alga, and seagrass. In contrast to previous studies, we detected no reduction in surface-area growth under future climate conditions compared with present day conditions. In terms of calcification, M. vertebralis’ epiphytic association to primary producers (i.e., calcifying algae and seagrasses) potentially ameliorates the effects of OA by buffering against declines in boundary layer pH during periods of photosynthesis (i.e., CO2 removal). Importantly for population maintenance, we observed a strong reduction in asexual fecundity under the 2100 scenario. We propose the additional energy needed to maintain growth might be one reason for drastically reduced asexual reproduction. The other possibility could be due to the +2°C temperature increase, which interfered with the environmental synchronization that triggered asexual multiple fission. We conclude that the low levels of reproduction will reduce populations in a high CO2 environment and reduce a valuable source of CaCO3 sediment production.