The dynamics of nitrogen (N) loss in the ocean’s oxygen-deficient zones (ODZs) are thought to be driven by climate impacts on ocean circulation and biological productivity. Here we analyze a data-constrained model of the microbial ecosystem in an ODZ and find that species interactions drive fluctuations in local- and regional-scale rates of N loss, even in the absence of climate variability. By consuming O ₂ to nanomolar levels, aerobic nitrifying microbes cede their competitive advantage for scarce forms of N to anaerobic denitrifying bacteria. Because anaerobes cannot sustain their own low-O ₂ niche, the physical O ₂ supply restores competitive advantage to aerobic populations, resetting the cycle. The resulting ecosystem oscillations induce a unique geochemical signature within the ODZ—short-lived spikes of ammonium that are found in measured profiles. The microbial ecosystem dynamics also give rise to variable ratios of anammox to heterotrophic denitrification, providing a mechanism for the unexplained variability of these pathways observed in the ocean.