The copepod Calanus hyperboreus, a key species of Arctic marine ecosystems, has a partially anoxic gut that is suspected to host anaerobic microbial activities. So far, however, only dead specimens have been studied in which gut processes are quickly abolished by microbial carcass degradation. Here, live specimens were exposed to different feeding regimes and ambient oxygen levels to study the controls on copepod-associated microbial nitrogen cycling in 15N-enrichment experiments. Algae-fed copepods exhibited consistently high rates of denitrification and low or variable rates of dissimilatory nitrate reduction to ammonium (or nitrite), nitrification, and nitrous oxide release. Thus, live C. hyperboreus contribute to pelagic fixed-nitrogen loss through denitrification that is otherwise absent from oxygenated Arctic surface waters. The feeding-related controls on copepod-associated anaerobic nitrogen cycling are supported by significantly reduced rates in starved copepods. In addition, freshly released fecal pellets showed similar patterns of nitrogen cycling as fed copepods. Unlike in previous studies on copepod carcasses, low ambient oxygen levels did not stimulate anaerobic nitrogen cycling in live specimens, supporting that the C. hyperboreus gut is anoxic, irrespective of ambient oxygen levels. Fecal pellets and carcasses retained denitrification activity for 4 d of simulated sinking. We estimate that during the time of the Arctic spring bloom, pelagic denitrification associated with live specimens, fecal pellets, and carcasses of C. hyperboreus is equivalent to ~12% of the benthic fixed-nitrogen loss. This estimate increases to ~28%, provided that the abundant sibling species C. glacialis and C. finmarchicus exhibit denitrification activities in proportion to their smaller body size.