Respiration is a key process in the cycling of particulate matter and, therefore, an important control mechanism of carbon export to the ocean's interior. Most of the fixed carbon is lost in the upper ocean, and only a minor amount of organic material sustains life in the deep-sea. Conditions are particularly extreme in hadal trenches, and yet they host active biological communities. The source of organic carbon that supports them and the contribution of these communities to the ocean carbon cycle, however, remain uncertain. Here we report on size-fractionated depth profiles of plankton respiration assessed from the activity of the electron transport system in the Atacama Trench region, and provide estimates of the minimum carbon flux (FC) needed to sustain the respiratory requirements from the ocean surface to hadal waters of the trench and shallower nearby sites. Plankton < 100 μm contributed about 90% to total community respiration, whose magnitude was highly correlated with surface productivity. Remineralization rates were highest in the euphotic zone and declined sharply within intermediate oxygen-depleted waters, remaining fairly constant toward the bottom. Integrated respiration in ultra-deep waters (> 1000 m) was comparable to that found in upper layers, with 1.3 ± 0.4 mmol C m−2 d−1 being respired in the hadopelagic. The comparison between our FC models and estimates of sinking particle flux revealed a carbon imbalance through the mesopelagic that was paradoxically reduced at greater depths. We argue that large fast-sinking particles originated in the overlying surface ocean may effectively sustain the respiratory carbon demands in this ultra-deep marine environment.