The adult Hydra polyp continuously renews all of its cells using three separate stem cell populations but the genetic pathways enabling these dynamic tissue properties are not well understood. We used Drop-seq to sequence 24,985 Hydra cells and identified the molecular signatures of a broad spectrum of cell states, from stem cells to terminally differentiated cells. We constructed differentiation trajectories for each cell lineage and identified the transcription factors expressed along these trajectories, thus creating a comprehensive map of all developmental lineages in the adult animal. We unexpectedly found that neuron and gland cell differentiation transits through a common progenitor state, suggesting a shared evolutionary history for these secretory cell types. Finally, we have built the first gene expression map of the Hydra nervous system. By producing a comprehensive molecular description of the adult Hydra polyp, we have generated a resource for addressing fundamental questions regarding the evolution of developmental processes and nervous system function. Overall design: Drop-seq analysis of homeostatic Hydra vulgaris AEP (24,985 cells, 15 Drop-seq libraries total, 13 libraries for whole animal dissociations, 2 libraries for suspensions enriched for neuronal cells using FACS), ATAC-seq analysis of whole homeostatic Hydra magnipapillata 105 (3 replicated ATAC-seq libraries), Tag-seq analysis of epithelium specific gene expression of homeostatic Hydra vulgaris AEP (3 replicates for body column endoderm, 3 replicates for body column ectoderm).