The inoculation of antibiotic-degrading bacteria into manure could promote the removal of antibiotics during composting. However, knowledge on the impact of inoculating these antibiotic-degrading bacteria on the composting process and indigenous microbial community succession is still limited. This study assessed the antibiotic removal efficiency in pig manure after inoculating a microbial inoculum with antibiotic-degrading bacteria as the key component. The effect of inoculating this microbial inoculum on the physicochemical dynamics and the succession of the manure bacterial community during composting was also analyzed. The results showed that the antibiotic degradation in pig manure reached 81.95% after inoculating the microbial inoculum. When compared with that in the control, the total concentration of antibiotic residues in manure with the microbial agent inoculated was decreased by 42.18%. During composting, inoculating the microbial inoculum accelerated the temperature rise of compost, favored water loss, and alleviated the release of NH3 and H2S. Moreover, the total nutrient content (nitrogen, phosphorus, and potassium) in the final compost and the germination index of radish seeds increased by 6.80% and 68.33%, respectively, after inoculating this microbial inoculum. Furthermore, inoculating the microbial inoculum increased the content of stable organic carbon in the final compost and decreased the content of recalcitrant substances such as cellulose and hemicellulose. The analysis of the manure bacterial community showed that inoculating the microbial inoculum increased the relative abundances of Actinomycetes and Firmicutes in the compost. In particular, the thermophilic bacteria that was positively related to the compost temperature was increased significantly (P<0.01) after inoculating the microbial inoculum, whereas the relative abundance of pathogenic bacteria was correspondingly decreased. Network analysis of the bacterial coexistence pattern showed that inoculating this microbial inoculum also changed the interaction pattern of indigenous manure bacterial communities, which greatly reduced the complexity and connectivity of the bacterial interaction and improved the ecological relationship between beneficial bacteria and other bacterial communities. The effect of this microbial inoculum on the interaction with manure bacterial community laid a foundation for the establishment of a new and healthier composting bacterial community. This study provides a scientific basis for the application and development of multifunctional antibiotic-degrading microbial agents in manure treatments.