The interactions between phytophagous insects and microorganisms allow the former to take advantage of plant tissue as a food resource, despite being nutritionally deficient and abundant in toxic metabolites. The West Indian fruit fly, Anastrepha obliqua (Macquart) (Diptera: Tephritidae), is a polyphagous species that feeds, as a larva, on the fruits of plants of various families. In Colombia, some of its hosts are red mombin (Spondias purpurea L.), mango (Mangifera indica L.) (both Anacardiaceae), and star fruit (Averrhoa carambola L.) (Oxalidaceae). We used whole metagenome sequencing (WMS) to characterize and compare the microbiota and microbiomes of A. obliqua larvae when they fed on these three fruits. The microbiota constituted of bacteria, fungi, and, to a lesser extent, archaea, and the number of microorganisms in each of these groups varied among host plants. On mango, the main group was Firmicutes; on star fruit and red mombin, Proteobacteria. In addition, on red mombin, fungal groups were more represented than on the other two fruits. For four dominant microbial species, Acetobacter persici Iino et al., Gluconobacter sphaericus (Ameyama) Malimas et al., Tatumella ptyseos Hollis et al., and Weissella confusa (Holzapfel & Kandler) Collins et al., the genomes were reconstructed. The annotation of these genomes allowed us to determine that A. persici, G. sphaericus, and T. ptyseos contain a large number of genes involved in amino acid metabolism pathways, whereas W. confusa contains many genes involved in carbohydrate metabolism pathways. These genes are important for the use of food resources, considering the poor nutritional composition of plant material. Our results form a starting point for understanding the contribution of microorganisms to the ability of A. obliqua to utilize its host plants, the evolutionary implications, and possible applications for the control of this pest insect.