White adipose tissue (WAT) can develop into several phenotypes with different pathophysiological impact on type 2 diabetes. To better understand the adipogenic process, the transcriptional events that occur during in vitro differentiation of human adipocytes were investigated and the findings linked to WAT phenotypes. Single molecule transcriptional profiling provided a detailed map of the expressional changes of genes, enhancers, and long non-coding RNAs, where different types of transcripts share common dynamics during differentiation. Common signatures include early down-regulated, transient, and late induced transcripts, all of which are linked to distinct developmental processes during adipogenesis. Enhancers expressed during adipogenesis overlap significantly with genetic variants associated with WAT distribution. Transiently and late-induced expressed genes are associated with hypertrophic WAT (few but large fat cells), a phenotype closely linked to insulin resistance and type 2 diabetes. Transcription factors that are expressed early or transiently affect differentiation and adipocyte function, and are controlled by several well-known upstream regulators such as glucocorticosteroids, insulin, cyclic AMP and thyroid hormones. Taken together, our results suggest a complex, but highly coordinated regulation of adipogenesis.