Rare studies investigated influence of neonicotinoid insecticides on the whole soil biota including non-target invertebrates and microorganisms. And less is known about the consequent intervention on soil C processes. This study aimed to decipher Collembola-fungi-bacteria interactive effects on pathways of maize C translocation, combining isotopic tracer analysis of relevant compartments with high-throughput sequencing for bacterial and fungal genetic profiles. Dinotefuran was applied at 0 or 100 μg kg⁻¹ (a simulating residual dosage) to microcosms containing soils, Collembola and ¹³C labelled maize. Dinotefuran drastically reduced the density and maize-derived biomass C of Collembola, while intensifying antagonistic associations between soil organisms, with flourishing growth of Ascomycota and Actinobacteria, e.g., Streptomyces. This led to higher soil organic C (SOC) mineralization (elevated by 9.8–10.5%) across soils, attributing to the shift in microbial taxonomic and functional guild, e.g., with the increased abundance of genes aligned to cytochrome P450. Maize decomposition was controlled by Collembola that primarily fed on maize, via grazing behavior that facilitated labile maize C preferred decomposers, e.g., Xanthomonadaceae. These findings elucidate the influence of minute dinotefuran on intra-linkages between biomes (Collembola, fungi and bacteria), and highlight such legacy effects on maize and SOC mineralization.