The Drosophila transcription factor (TF) Zfh1 has distinct roles compared to the cell lineage‐determining TFs in almost all mesoderm‐derived tissues. Here, we link Zfh1 to the well‐characterized mesodermal transcriptional network. We identify five enhancers integrating upstream regulatory inputs from mesodermal TFs and directing zfh1 expression in mesoderm. Most downstream Zfh1‐target genes are co‐bound by mesodermal TFs, suggesting that Zfh1 and mesodermal TFs act on the same sets of co‐regulated genes during the development of certain mesodermal tissues. Furthermore, we demonstrate that Zfh1 is critical for the expression of a hemocyte marker gene peroxidasin and helps restrict the activity of a hemocyte‐specific enhancer of serpent to hemocyte‐deriving head mesoderm, suggesting a potential role of Zfh1 in hemocyte development.