Both the quality of chicken meat and the quality of chicks are influenced by the level of breast muscle glycogen reserves. In order to study the role of digestive metabolism in establishing this muscular phenotype, we compared two divergent chicken lines for the ultimate pH (pHu) of the breast meat, a proxy for glycogen reserves. Males aged 4 weeks had twice the breast muscle glycogen content in the pHu- line (low pHu) than in the pHu + line (high pHu). The increase in glycogen reserves (pHu-) was associated with a higher relative weight of the proventriculus and gizzard, as well as better apparent ileal digestibility of nitrogen and calcium. The diversity of the cecal microbiota was comparable, but three bacterial genera (Lachnospira, Lachnospiraceae UCG-010, Caproiciproducens) varied between the lines. The differences observed could lead to down-regulation of carbon fixation in prokaryotes and of the citrate cycle in the pHu + line. RNA-seq analysis of the jejunum, the major site of nutrient absorption, revealed 149 genes differentially expressed (DE) between the lines, including several genes linked to immunity, hormonal response and circadian rhythms that are less expressed in pHu + animals. Others involved in cell migration and proliferation, and more generally tissue morphogenesis, also differed between the lines. Among the DE genes, several co-localized with Quantitative Trait Loci (QTL) controlling pHu and selection signatures identified in the divergent lines, such as the gene coding for ghrelin, a hormone regulating appetite.