The microbiota stimulates inflammation, but the signaling pathways and the members of the microbiota involved remain poorly understood. We found that the microbiota induces interleukin-1β (IL-1β) release upon intestinal injury and that this is mediated via the NLRP3 inflammasome. Enterobacteriaceae and in particular the pathobiont Proteus mirabilis, induced robust IL-1β release that was comparable to that induced by the pathogen Salmonella. Upon epithelial injury, production of IL-1β in the intestine was largely mediated by intestinal Ly6Chigh monocytes, required chemokine receptor CCR2 and was abolished by deletion of IL-1β in CCR2+ blood monocytes. Furthermore, colonization with P. mirabilis promoted intestinal inflammation upon intestinal injury via the production of hemolysin, which required NLRP3 and IL-1 receptor signaling in vivo. Thus, upon intestinal injury, selective members of the microbiota stimulate newly recruited monocytes to induce NLRP3-dependent IL-1β release, which promotes inflammation in the intestine. Display omitted •Distinct commensal bacteria induce IL-1β via the NLRP3 inflammasome•The pathobiont Proteus mirabilis induces robust IL-1β via the NLRP3 inflammasome•Recruited monocytes are required for commensal induced IL-1β production•IL-1β induced by commensals promotes intestinal inflammation via NLRP3 Interleukin-1β (IL-1β) is a major inflammatory cytokine induced during colitis, but how the microbiota regulate this cytokine is largely unknown. Nunez and colleagues show that IL-1β is produced by recruited monocytes in response to selective commensals to promote colitis upon intestinal damage.