The cycling of carbon (C) by benthic organisms is a key ecosystem function in the deep sea. Pulse-chase experiments are designed to quantify this process, yet few studies have been carried out using abyssal (3500–6000 m) sediments and only a handful of studies have been undertaken in situ. We undertook eight in situ pulse-chase experiments in three abyssal strata (4050–4200 m water depth) separated by tens to hundreds of kilometers in the eastern Clarion-Clipperton Fracture Zone (CCFZ). These experiments demonstrated that benthic bacteria dominated the consumption of phytodetritus over short (~ 1.5 d) time scales, with metazoan macrofauna playing a minor role. These results contrast with the only other comparable in situ abyssal study, where macrofauna dominated phytodetritus assimilation over short (2.5 d) time scales in the eutrophic NE Atlantic. We also demonstrated that benthic bacteria were capable of converting dissolved inorganic C into biomass and showed that this process can occur at rates that are as high as the bacterial assimilation of algal-derived organic C. This demonstrates the potential importance of inorganic C uptake to abyssal ecosystems in this region. It also alludes to the possibility that some of the C incorporation by bacteria in our algal-addition studies may have resulted from the incorporation of labeled dissolved inorganic carbon initially respired by other unstudied organisms. Our findings reveal the key importance of benthic bacteria in the short-term cycling of C in abyssal habitats in the eastern CCFZ and provide important information on benthic ecosystem functioning in an area targeted for commercial-scale, deep-sea mining activities.