Abstract We developed a comprehensive molecular atlas of human granulopoiesis, encompassing the transcriptome (mRNA), proteome, and non-coding RNA (miRNA, lncRNA) of seven defined stages of neutrophil maturation. Two waves of mRNA transcription activity were observed. Whereas the first wave, extending from myeloblasts to metamyelocytes, showed correlated mRNA transcripts and protein translation, the second wave was characterized by uncoupling of transcription and translation. Integrated analysis revealed intricate dynamics of transcription and translation parallelization in granule subset proteins, ribosomes, and mitochondria, respectively. We identified the hsa-miR-106a-5p family and hsa-miR-125a-5p as potential repressors of myeloid differentiation in myeloblasts, and hsa-miR-193a-5p as a repressor of the SWI/SNF complex. LncRNA transcripts displayed remarkable stage specificity. Whereas NEAT1 and MAILR were expressed only from the band stage onwards, ITGB2-AS1 was expressed exclusively in metamyelocytes. Novel lncRNAs with high expression were found in the terminal S-stage and PMN (ENSG00000288819, ENSG00000203644). A comprehensive analysis of transcription factor signatures, including activity on target genes, revealed previously unrecognized factors as well as a yet underappreciated transcriptional role of lactotransferrin (LTF) in early maturation stages. Characterization of single-cell-clusters via transcriptional profiles of histologically defined maturation stages enabled stage-specific cell labeling. To ensure the availability of our data and the reproducibility of our analysis, our complete datasets, analysis codes and online tool for exploration are available on www.granulopoiesis.com.