During the growth and development of animals, there is an interaction between the gut microbiota and the host genotype. The host genotype can regulate the microbiota, and in turn, the microbiota can influence host gene expression, thereby affecting the animal's production performance. This study explored the dynamic interplay between the gut microbiota and host gene expression in body weight variation in Dagu chicken, an indigenous poultry genetic resource in China. We characterized mucosa-associated microbiota across four gastrointestinal segments (duodenum, jejunum, ileum, cecum) and ileocecal chyme microbiota in 12-week-old Dagu chickens stratified by divergent body weight phenotypes, while simultaneously quantifying region-specific intestinal epithelial transcriptional regulation. 16S rDNA sequencing was employed to identify Firmicutes as the predominant bacterial phylum, with notable differences in the abundance of specific genera (e.g., Ligilactobacillus and Lactobacillus) being observed between the high- or low-body-weight groups. Enhanced biosynthesis pathways were functionally predicted in heavier roosters, whereas reduced nutrient metabolism pathways were contrasted. A conserved functional concordance was observed between regionally predominant differential microbiota and the physiological specialization of corresponding intestinal niches. Functional analysis revealed that the high-body-weight group demonstrated superior capabilities in microbial biosynthesis, whereas the low-body-weight group exhibited enhanced microbial metabolic activity. NAA80 was identified as the common differentially expressed gene across all intestinal epithelial tissues. The Gene Ontology and KEGG pathway analyses revealed elevated nutrient absorption efficiency in the high-body-weight group, while the low-body-weight group demonstrated accelerated cellular renewal rates and shorter cycles. Correlation analysis identified significant associations between gut microbiota and host genes expression profiles, with the majority of correlations being positive. These results suggest a coordinated interaction between microbial communities and host genetic regulation, potentially driving phenotypic differences in body weight performance.