Terrestrial microorganisms have long been recognised as key players in nutrient cycles, and untangling their functions within the agricultural plant-soil nexus are paramount for futureproofing Australian agriculture. Whilst their roles in nitrogen, phosphorus and carbon cycling are well described, less is known about their effects on the cycling of the atmospheric trace gas, hydrogen (H2). Within agroecosystems, a primary source of H2 is as a by-product of nitrogen fixation, with legumes often associated with a temporary supersaturation of H2 around legume nodules. The temporary nature suggests that the H2 produced is rapidly recycled by closely associated microorganisms or internally if they harbour high-affinity uptake hydrogenases. Using a multidisciplinary approach, we combined traditional gas chromatography, metagenomics and metatranscriptomics to characterise the effect of exogenous fertiliser addition on the resilience of agroecosystem H2 oxidation as well as other nutrient cycling processes. Five agricultural soils with diverse physicochemical properties were assessed for their ability to oxidise two concentrations of H2 within microcosms. All soils were able to rapidly oxidise the excess concentration of H2 (10,000 ppmv) to close to atmospheric levels, albeit at different rates, suggesting that soil physicochemical properties play a key role in H2 uptake rate. In a soil microcosm amended with excess H2, fertiliser or a combination, the soil’s uptake was robust, with only a slight increase in uptake lag time observed for the combined condition. Metagenomic and metatranscriptomic profiling highlighted that the predominant hydrogenase is the persistence-linked group 1h [NiFe] and that expression increased in the presence of both excess H2 and the combined fertiliser+H2 condition. Moreover, key nitrogen cycling processes, including ammonia oxidation and nitrite reduction, were also enriched in the presence of the combined fertiliser+H2 condition, suggesting that there is possibly a synergistic relationship between nitrogen and hydrogen cycling microorganisms. Thus, understanding the role hydrogen cycling plays in agricultural soils as well as how this and other metabolic processes are affected is crucial for the future development of novel and sustainable agricultural practices with microorganisms at the forefront.