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.