Dietary prunes preserve bone mineral density in postmenopausal women, prevent glucocorticoid-induced bone loss in mice, and enhance trabecular bone volume in healthy male and female mice. Prune intake also alters the gut microbiome composition. The microbial metabolites that connect prune intake to bone phenotypes in healthy hosts remain unclear. Metagenomic data from our glucocorticoid-induced bone loss model identified Anaerostipes caccae (A. caccae) as a bacteria whose gut levels are induced by a prune diet. Guided by this, we examined A. caccae metabolites and their connection with diet, gut microbial communities and bone phenotypes. To identify prune metabolites, we cultured A. caccae in one of four media (RCM, RCM plus glucose, and RCM plus prune) and profiled exometabolites by untargeted metabolomics. We then mapped these bacterial metabolites onto serum features and trabecular bone volume changes in mice receiving a 4-week 25% w/w prune diet. In A. caccae cultures we detect more than 1,000 exometabolite features. Prune-containing media show higher exometabolite diversity than non-prune media (mean Shannon index 5.2 versus 4.6, p < 0.001), and principal coordinate analysis separates prune and non-prune media. A random forest model on A. caccae exometabolite data identifies a small set of discriminant metabolites that are also elevated in the serum of prune-fed mice. In sum, we identify prune-enriched microbial metabolites that A. caccae produces in vitro and validate their presence and response to prune in vivo. We further link them to increased trabecular bone volume, supporting microbiome-focused metabolite strategies to enhance skeletal health.