Understanding the development of functional attributes of host-associated microbial communities is essential for developing novel microbe-based solutions for sustainable animal production. We applied multi-omics to 388 broiler chicken caecal samples to characterise and model the functional dynamics of 822 bacterial strains. Although microbial community diversity metrics increased with chicken age as expected, the overall metabolic capacity and activity of the microbiota exhibited an unexpected decrease. This drop occurred due to the spread of non-culturable clades with small genomes and low metabolic capacities, including RF39, RF32, and UBA1242. The intensity of this decrease was associated with animal growth, whereby chickens with higher abundances of low-capacity bacteria exhibited higher body weights. This previously unreported link between metabolic capacity of microbes and animal body weight suggests a relevant role of non-culturable bacteria with reduced-genomes for host biology, and opens new avenues in the search for microbe-based solutions to improve sustainability of animal production.