Adult organisms must sense and adapt to environmental fluctuations. In high-turnover tissues such as the intestine, these adaptive responses require rapid changes in gene expression that, in turn, likely involve posttranscriptional gene control. However, intestinal-tissue-specific microRNA (miRNA)-mediated regulatory pathways remain unexplored. Here, we report the role of an intestinal-specific miRNA, , that non-cell autonomously regulates stem cell numbers during tissue homeostasis and regeneration in the adult midgut. We identify its downstream target , the ortholog of mammalian KLF10/11 transcription factors, which mediates this function by promoting paracrine enterocyte-to-stem-cell bone morphogenetic protein (BMP) signaling. We also show that mature levels transiently decrease in response to stress and that this decrease is required for proper stem cell expansion during tissue regeneration. In summary, we have identified a posttranscriptional mechanism that modulates BMP signaling activity within adult intestinal tissue during both normal homeostasis and tissue regeneration to regulate intestinal stem cell numbers.