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.Enterobacteriaceaeand in particular the pathobiontProteus mirabilis, induced robust IL-1β release that was comparable to that induced by the pathogenSalmonella. Upon epithelial injury, production of IL-1β in the intestine was largely mediated by intestinal Ly6Chighmonocytes, required chemokine receptor CCR2 and was abolished by deletion of IL-1β in CCR2+blood monocytes. Furthermore, colonization withP. mirabilispromoted 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.