Understanding the dynamic and stability of gut microbiota over the course of production cycle of broiler chicken can help identify microbial features that associate with better health and productivity. In the present study, we profile the changes in the composition and stability of gut microbiota of commercially raised broilers at nine distinct time points using shotgun metagenomics and culturomics approaches. We demonstrate, within the first week post-hatching, a rapid decline in relative abundance of 122 pioneer microbial species including Bacteroides fragilis, Lachnospira eligens and Ruminococcus gnavus, accompanied by a substantial decrease in both microbial richness and diversity. This was followed by a gradual increase and stabilization in the microbial diversity and population structure that persisted until the broilers reached the marketing age. Throughout the production cycle, key bacterial families such as Lachnospiraceae, Bacteroidaceae, and Ruminococcaceae were identified. However, significant shifts at the lower taxonomic levels occurred at different production stages, influencing the functional capacities and resistance profiles of the microbiota. During the rapid growth phase, enzymes crucial to vitamin and amino acid metabolism dominated, whereas enzymes associated with carbohydrate and energy metabolism were notably more abundant during the fattening stage. Many predicted antibiotic resistance genes were detected in association with typical commensal bacterial species in the gut microbiota, indicating a sustained resistance of the gut microbiota to antibiotic classes such as aminoglycosides and tetracyclines, which persist even in the absence of antibiotic selection pressure. Our research carries important implications for the management and health surveillance of broiler production.