Increasing evidence indicate that transcription factors (TFs) play an essential role in specifying cell identities. Here, we report the identification of a transcriptional network that maintains intestinal stem cells (ISCs) in Drosophila adult midgut. The core module of the network consists of FoxA TF Fkh, E-protein TF Da and SoxE TF dSox9. Our genetic analyses indicate that the ISCs defective in these TFs rapidly lose their progenitor fates. On the other hand, their ectopic inductions in the progenitors prevent them from differentiating into mature gut cells. We mapped their binding sites in the progenitors and revealed that they bind to many of the same genomic loci and likely regulate a common set of target genes including themselves. In addition, we showed that TFs downstream of several key ISC niche pathways and epigenetic regulators also bind to these same genomic loci. And these shared genomic loci likely function as active enhancers and mediate the induction of progenitor genes. Finally, we explored the interaction between the core module and niche pathways and demonstrated that dSox9 primes Jak-Stat pathway for activation in the progenitors, which in turn induces Emc to suppress Da to promote midgut differentiation.