Successfully adapting to a feral lifestyle with different access to food, shelter and other resources requires rapid physiological and behavioural changes, which could potentially be facilitated by gut microbiota plasticity. To investigate whether alterations in gut microbiota support this transition to a feral lifestyle, we analysed the gut microbiomes of domestic and feral cats from six geographically diverse locations using genome-resolved metagenomics. By reconstructing 229 non-redundant metagenome-assembled genomes from 92 cats, we identified a typical carnivore microbiome structure, with notable diversity and taxonomic differences across regions. While overall diversity metrics did not differ significantly between domestic and feral cats, hierarchical modelling of species communities, accounting for geographic and sex covariates, revealed significantly larger microbial functional capacities among feral cats. The increased capacity for amino acid and lipid degradation corresponds to feral cats' dietary reliance on crude protein and fat. A second modelling analysis, using behavioural phenotype as the main predictor, unveiled a positive association between microbial production of short-chain fatty acids, neurotransmitters and vitamins and cat aggressiveness, suggesting that gut microbes might contribute to heightened aggression and elusiveness observed in feral cats. Functional microbiome shifts may therefore play a significant role in the development of physiological and behavioural traits advantageous for a feral lifestyle, a hypothesis that warrants validation through microbiota manipulation experiments.