Termites digest lignocellulose with the help of their symbiotic gut microbiota. In the hindgut of evolutionary lower termites, a dense community of cellulolytic flagellates sequesters wood particles from the hindgut content into their digestive vacuoles. In higher termites (family Termitidae), which possess an entirely prokaryotic microbiota, the wood particles are available for bacterial colonization. Substantial particle‐associated cellulase activities have been detected in the hindgut of Nasutitermes species, but the microorganisms responsible for these activities and their potential association with the wood fibres remain to be studied. Here, we used density‐gradient centrifugation to separate wood fibres and adherent bacterial cells from cells freely suspended in the hindgut fluid. In Nasutitermes corniger, the fibre fraction contained 28% of the DNA and 45% of the cellulase activity in the luminal contents (P3 region). Community fingerprinting (terminal restriction fragment length polymorphism) and pyrotag sequencing analysis of the bacterial 16S rRNA genes demonstrated that the wood fibres in the hindgut of both N. corniger and N. takasagoensis are specifically colonized by members of Fibrobacteres, the TG3 phylum, and certain lineages of Spirochaetes characteristic of the gut microbiota of wood‐feeding higher termites. We propose that the loss of flagellates in higher termites provided a new niche for fibre‐associated cellulolytic bacteria.