<p><i>Antheraea assamensis</i> Helfer is an economically important, endemic, lepidopteran insect native to Northeast India that produces a lustrous golden-coloured silk of distinct quality and durability. To date, the gut microbiota of <i>A. assamensis</i> has remained largely unexplored. The present work aimed to comprehensively identify and characterize the gut microbial community of <i>A. assamensis</i> through culture-independent approach. The gene expression analysis of the gut microbial community was studied through metatranscriptomic analysis. The influence of the host leaf-associated microbiota on larval gut microbial composition and its variation to changes in host plant was also investigated. The results have identified over 30 bacterial and archaeal phyla indicating a highly diverse gut microbial community of <i>A. assamensis</i> dominated by Proteobacteria (25.78%), Patescibacteria (12.77%), Planctomycetota (12.66%), Chloroflexi (8.63%), Acidobacteria (6.85%) and Actinobacteria (3.39%). Functional analysis of <i>A. assamensis</i> gut microbiota through shotgun metagenomic and metatranscriptomic investigation revealed key associations between the insect and its gut microbial community including host leaf digestion, metabolite detoxification, chitinase production and fat body metabolism. The host leaf-associated microbiota was found to occupy a major portion of the total larval gut microbiota. However, the diversity of the larval gut microbiota was greater than the host leaf-associated microbiota. The findings of this study will illustrate the structure of the gut microbial community of <i>A. assamensis</i>, their key interactions with the host organism and the role of host leaf-associated microbiota on the holobiont.</p> Graphical Abstract <p></p>