Mass rearing the black soldier fly, , for waste bioremediation and valorisation is gaining traction on a global scale. While the health and productivity of this species are underpinned by associations with microbial taxa, little is known about the factors that govern gut microbiome assembly, function, and contributions towards host phenotypic development in actively feeding larvae. In the present study, a 16S rDNA gene sequencing approach applied to a study system incorporating both feed substrate and genetic variation is used to address this knowledge gap. It is determined that the alpha diversity of larval gut bacterial communities is driven primarily by features of the larval feed substrate, including the diversity of exogenous bacterial populations. Microbiome beta diversity, however, demonstrated patterns of differentiation consistent with an influence of diet, larval genetic background, and a potential interaction between these factors. Moreover, evidence for an association between microbiome structure and the rate of larval fat accumulation was uncovered. Taxonomic enrichment analysis and clustering of putative functional gut profiles further suggested that feed-dependent turnover in microbiome communities is most likely to impact larval characteristics. Taken together, these findings indicate that host-microbiome interactions in this species are complex yet relevant to larval trait emergence.