The epithelial and interstitial stem cells of the freshwater polypHydraare the best characterized stem cell systems in any cnidarian, providing valuable insight into cell type evolution and the origin of stemness in animals. However, little is known about the transcriptional regulatory mechanisms that determine how these stem cells are maintained and how they give rise to their diverse differentiated progeny. To address such questions, a thorough understanding of transcriptional regulation inHydrais needed. To this end, we generated extensive new resources for characterizing transcriptional regulation inHydra, including new genome assemblies forHydra oligactisand the AEP strain ofHydra vulgaris, an updated whole-animal single-cell RNA-seq atlas, and genome-wide maps of chromatin interactions, chromatin accessibility, sequence conservation, and histone modifications. These data revealed the existence of large kilobase-scale chromatin interaction domains in theHydragenome that contain transcriptionally co-regulated genes. We also uncovered the transcriptomic profiles of two previously molecularly uncharacterized cell types, isorhiza-containing nematocytes and somatic gonad ectoderm. Finally, we identified novel candidate regulators of cell-type-specific transcription, several of which have likely been conserved at least since the divergence ofHydraand the jellyfishClytia hemisphaericaover 400 million years ago.