The vast majority of genetic variants associated with complex human traits map to non-coding regions, but little is understood about how they modulate gene regulation in health and disease. Here, we analyzed Assay for Transposase-Accessible Chromatin (ATAC-seq) profiles from activated primary CD4+ T cells of 105 healthy donors to identify ATAC-QTLs: genetic variants that affect chromatin accessibility. We found that ATAC-QTLs are widespread, disrupt binding sites for transcription factors known to be important for CD4+ T cell differentiation and activation, overlap and mediate expression QTLs from the same cells and are enriched for SNPs associated with autoimmune diseases. We also identified numerous pairs of ATAC-peaks with highly correlated chromatin accessibility. When we characterize 3D chromosome organization in primary CD4+ T cells by in situ-Hi-C, we found that correlated peaks tend to reside in the same chromatin contact domains, span super-enhancers, and are more impacted by ATAC-QTLs than single peaks. Thus, variability in chromatin accessibility in primary CD4+ T cells is heritable, is determined by genetic variation in a manner affected by the 3D organization of the genome, and mediates genetic effects on gene expression. Our results provide insights into how genetic variants modulate chromatin state and gene expression in primary immune cells that play a key role in many human diseases.