A deeper understanding of the microbial community structure is very important in bioremediation for polychlorinated dibenzo-p-dioxins/dibenzofurans (PCDD/Fs). However, this has been insufficiently addressed in previous studies. To obtain more information, we pyrosequenced the V4/V5 regions of the 16S rRNA genes of bacterial communities transited from polluted soil to batch microcosms that rapidly degraded high concentrations of octachlorodibenzofuran (OCDF). The analysis results contained an average of 11,842 reads per sample, providing the first detailed description of bacterial communities associated with PCDD/Fs. The community composition markedly changed to be concomitant with the degradation of OCDF, indicating that a distinctive population structure developed rapidly in the microcosm. Although oxygen gas was provided weekly to the microcosm, the growth of potential degraders, Sphingomonas, Pseudomonas, Rhodococcus, and Clostridium, was observed, but in consistently low quantities. While anaerobic Sedimentibacter initially emerged as an abundant pioneer, several aerobic participants, such as the genera Brevundimonas, Pseudoxanthomonas, and Lysobacter, exhibited a large increase in their 16S rRNA gene copies within the timeframe, which showed a temporal population dynamic, and indicated their collaborative contributions to the degradation of OCDF under hypoxic conditions. These results have provided a deeper insight into the microbial community structure and population dynamics of the OCDF-degrading microcosm.