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Endothelial‐to‐hematopoietic transition (EHT) is an important stage in definitive hematopoietic development. However, the genetic mechanisms underlying human EHT remain poorly characterized. We performed single cell RNA‐seq using 55 hemogenic endothelial cells (HECs: CD31 + CD144 + CD41 – CD43 – CD45 – CD73 –  RUNX1c  + ), 47 vascular endothelial cells without hematopoietic potential (non‐HE: CD31 + CD144 + CD41 – CD43 – CD45 – CD73 –  RUNX1c  – ), and 35 hematopoietic progenitor cells (HPCs: CD34 + CD43 +  RUNX1c  + ) derived from human embryonic stem cells (hESCs). HE and HP were enriched in genes implicated in hemogenic endothelial transcriptional networks, such as  ERG ,  GATA2 , and  FLI . We found transcriptional overlap between individual HECs and HPCs; however, these populations were distinct from non‐HE. Further analysis revealed novel biomarkers for human HEC/HPCs, including  TIMP3 ,  ESAM ,  RHOJ , and  DLL4 . Collectively, we demonstrate that hESC‐derived HE and HP share a common developmental pathway, while non‐HE are more heterogeneous and transcriptionally distinct. Our findings provide a novel strategy to test new genetic targets and optimize the production of definitive hematopoietic cells from human pluripotent stem cells. S tem  C ells   2018;36:206–217

Single Cell Resolution of Human Hematoendothelial Cells Defines Transcriptional Signatures of Hemogenic Endothelium