Long-range interactions between regulatory elements and gene promoters play key roles in transcriptional regulation. The vast majority of interactions are uncharted, constituting a major missing link in understanding genome control. Here, we use promoter capture Hi-C to identify interacting regions of 31,253 promoters in 17 human primary hematopoietic cell types. We show that promoter interactions are highly cell type specific and enriched for links between active promoters and epigenetically marked enhancers. Promoter interactomes reflect lineage relationships of the hematopoietic tree, consistent with dynamic remodeling of nuclear architecture during differentiation. Interacting regions are enriched in genetic variants linked with altered expression of genes they contact, highlighting their functional role. We exploit this rich resource to connect non-coding disease variants to putative target promoters, prioritizing thousands of disease-candidate genes and implicating disease pathways. Our results demonstrate the power of primary cell promoter interactomes to reveal insights into genomic regulatory mechanisms underlying common diseases. Display omitted •High-resolution maps of promoter interactions in 17 human primary blood cell types•Interaction patterns are cell type specific and segregate with the hematopoietic tree•Promoter-interacting regions enriched for regulatory chromatin features and eQTLs•Promoter interactions link non-coding GWAS variants with putative target genes This study deploys a promoter capture Hi-C approach in 17 primary blood cell types to match collaborating regulatory regions and identify genes regulated by noncoding disease-associated variants. Explore this and other papers at the Cell Press IHEC webportal at http://www.cell.com/consortium/IHEC.