Dietary digestion-resistant starch (RS) provides health benefits to the host via gut microbiome-mediated metabolism. The degree to which cats manifest beneficial changes in response to RS intake was examined. Healthy cats (N = 36) were fed identically formulated foods processed under high (n = 17) or low (n = 19) shear extrusion conditions (low and high RS levels [LRS and HRS], respectively). Fecal samples collected after 3 and 6 weeks' feeding were assayed for stool firmness score, short-chain fatty acids, ammonia, and changes to the global metabolome and microbiome; fecal immunoglobulin A (IgA) was analyzed at week 6. Few differences were seen in proximate analyses of the foods; stool firmness scores did not differ. In cats consuming HRS food, concentrations of fecal butyrate and the straight chain:branched chain fatty acid ratio were significantly greater in feces at both weeks 3 and 6, while fecal ammonia was reduced at week 6 relative to feces from LRS-fed cats. Fecal IgA concentrations were significantly higher at week 6 with HRS food. RS consumption altered 47% of the fecal metabolome; RS-derived sugars and metabolites associated with greater gut health, including indoles and polyamines, increased in the cats consuming HRS food relative to those fed the LS food, while endocannabinoid N-acylethanolamines decreased. Consumption of HRS food increased concentrations of the ketone body 3-hydroxybutyrate in feces and elevated concentrations of reduced members of NADH-coupled redox congeners and NADH precursors. At the microbiome genus-level, 21% of operational taxonomic units were significantly different between food types; many involved taxa with known saccharolytic or proteolytic proclivities. Microbiome taxa richness and Shannon and Simpson alpha diversity were significantly higher in the HRS group at both weeks. These data show that feline consumption of grain-derived RS produces potentially beneficial shifts in microbiota-mediated metabolism and increases IgA production.