Plant productivity and other ecosystem functions often increase with plant diversity at a local scale. Alongside various plant-centered explanations for this pattern, there is accumulating evidence that multi-trophic interactions shape this relationship. Here, we investigated for the first time if plant diversity effects on ecosystem functioning are mediated or driven by decomposer animal diversity and identity using a double-diversity microcosm experiment. We show that many ecosystem processes and ecosystem multifunctionality (herbaceous shoot biomass production, litter removal, and N uptake) were affected by both plant and decomposer diversity, with ecosystem process rates often being maximal at intermediate to high plant and decomposer diversity and minimal at both low plant and decomposer diversity. Decomposers relaxed interspecific plant competition by enlarging chemical (increased N uptake and surface-litter decomposition) and spatial (increasing deep-root biomass) habitat space and by promoting plant complementarity. Anecic earthworms and isopods functioned as key decomposers; although decomposer diversity effects did not solely rely on these two decomposer species, positive plant net biodiversity and complementarity effects only occurred in the absence of isopods and the presence of anecic earthworms. Using a structural equation model, we explained 76% of the variance in plant complementarity, identified direct and indirect effect paths, and showed that the presence of key decomposers accounted for approximately three-quarters of the explained variance. We conclude that decomposer animals have been underappreciated as contributing agents of plant diversity–ecosystem functioning relationships. Elevated decomposer performance at high plant diversity found in previous experiments likely positively feeds back to plant performance, thus contributing to the positive relationship between plant diversity and ecosystem functioning.