The invasive fall armyworm, Spodoptera frugiperda (J.E. Smith; Lepidoptera: Noctuidae), is considered one of the most harmful pests in corn, rice and cotton crops and has developed resistance to the most widespread methods used to control it, chemical insecticides and transgenic crops based on Bt toxins. On the other hand, gut microbiota plays an important role in the insect's fitness, and metatranscriptomic analyses of the insect host are an invaluable tool for identifying new pest control targets. Notwithstanding, there are extremely few reports on the functionally active profile of the gut microbiota in insects, especially in lepidopterans. Moreover, most studies have only described the bacterial community even though all the components of the microbiota, Bacteria, Archaea, fungi, protozoa and viruses, influence different physiological aspects of the insect host. This is the first time an unbiased and comprehensive metatranscriptomic approach has been used to describe the taxonomic and functional profile of the gut microbiota of S. frugiperda larvae, both bacterial and non‐bacterial. We identified novel and very active components which were putatively playing an important nutritional role, such as ammonia‐oxidizing Archaea and Bacteria, and a xylan‐ and hemicellulose‐degrading Actinobacteria. This analysis also allowed us to identify potential biocontrol agents.