The bioavailability of essential nutrients such as nitrogen and phosphorus has fluctuated with the chemical evolution of Earth surface environments over geological timescales. However, significant uncertainty remains over the evolution of Earth’s early nitrogen cycle, particularly how and when it responded to the evolution of oxygenic photosynthesis. Here we apply multi-proxy geochemical analyses (Fe speciation, δ13C and δ15N) to exceptionally well-preserved shales from the approximately 2.7 billion year old Manjeri Formation in the Belingwe Greenstone Belt, Zimbabwe, to evaluate the redox status of Earth’s early nitrogen cycle and decipher feedbacks associated with the initial stages of planetary oxygenation. These continental shelf sediments were previously linked to early cyanobacterial oxygen production, and provide a direct test of conflicting hypotheses concerning the importance of nitrogen oxyanions in the Late Archaean era. Our data reveal a dominantly anaerobic marine nitrogen cycle in which ammonium-replete ferruginous waters underlay an ephemeral oxygen oasis. Driven by the emergence of oxygenic photosynthesis, increased primary productivity could have periodically strengthened export production, which allowed for the accumulation of ammonium in the water column during organic matter degradation. Restricted oxygen availability could have allowed the upwelling ammonium to reach the photic zone to provide ample nitrogen to fuel a prolific Late Archaean biosphere. Biologically available nitrogen in the form of ammonium was abundant in the Late Archaean ocean, according to nitrogen isotope and proxy analyses on 2.7 billion year old shales from Zimbabwe.