Pluripotent stem cells are capable of unlimited self-renewal and can give rise to specialised cell types based on stepwise changes in the transcriptional networks that orchestrate complex fate choices from pluripotency into differentiated states. While transcriptional profiling has been a central endpoint for analyzing pluripotency, the heterogeneity of cell states represented in pluripotent cultures has not been described at a global transcriptional level. Since each cell has a unique expression state comprising a particular repertoire of regulatory factors and target gene behavior, single-cell RNA sequencing (scRNA-seq) can be used to gain a transcriptome-level understanding of how individual cells function in pluripotency. In this study, we provide the largest single cell transcriptional profiling of undifferentiated human pluripotent stem cells currently available which cumulatively amount to 18,787 cells. Using scRNA-seq, we show that iPS cells exist in 4 distinct stages of pluripotency: (i) proliferative, (ii) quiescent, (iii) early primed for differentiation and (iv) late-primed for differentiation.