Rising ocean temperatures affect marine microbial ecosystems directly, since metabolic rates (e.g. photosynthesis, respiration) are temperature-dependent, but temperature also has indirect effects mediated through changes to the physical environment. Empirical observations of the long-term trends in biomass and productivity measure the integrated response of these two kinds of effects, making the independent components difficult to disentangle. We used a combination of modeling approaches to isolate the direct effects of rising temperatures on microbial metabolism and explored the consequences for food web dynamics and global biogeochemistry. We evaluated the effects of temperature sensitivity in two cases: first, that all metabolic processes have the same temperature sensitivity, and alternatively, that heterotrophic processes have higher temperature sensitivity than autotrophic processes. No other study has explored the direct effects of temperature on ecosystem provisioning (primary productivity, biomass, export) independently of the associated changes to the physical environment that result from warming. Microbial ecosystems at higher temperatures are characterized by increased productivity, but decreased biomass stocks as a result of transient, high export events that remove biomass from the surface ocean. Trophic dynamics also mediate changes to community size structure, resulting in longer food chains and increased mean body size at higher temperatures. These ecosystem thermal responses are magnified when the temperature sensitivity of heterotrophs is higher than that of autotrophs. These results provide important context for understanding the combined food web response to direct and indirect temperature effects and inform the construction and interpretation of Earth systems models used in climate projections.