Dryocosmus kuriphilus (Hymenoptera: Cynipidae) induces galls on chestnut trees, which results in massive yield losses worldwide. Torymus sinensis (Hymenoptera: Torymidae) is a host-specific parasitoid that phenologically synchronizes with D. kuriphilus. Bacteria play important roles in the life cycle of galling insects. The aim of this research is to investigate the bacterial communities and predominant bacteria of D. kuriphilus, T. sinensis, D. kuriphilus galls and the galled twigs of Castanea mollissima. We sequenced the V5–V7 region of the bacterial 16S ribosomal RNA in D. kuriphilus, T. sinensis, D. kuriphilus galls and galled twigs using high-throughput sequencing for the first time. We provide the first evidence that D. kuriphilus shares most bacterial species with T. sinensis, D. kuriphilus galls and galled twigs. The predominant bacteria of D. kuriphilus are Serratia sp. and Pseudomonas sp. Furthermore, the bacterial community structures of D. kuriphilus and T. sinensis clearly differ from those of the other groups. Many species of the Serratia and Pseudomonas genera are plant pathogenic bacteria, and we suggest that D. kuriphilus may be a potential vector of plant pathogens. Furthermore, a total of 111 bacteria are common to D. kuriphilus adults, T. sinensis, D. kuriphilus galls and galled twigs, and we suggest that the bacteria may transmit horizontally among D. kuriphilus, T. sinensis, D. kuriphilus galls and galled twigs on the basis of their ecological associations.