Genome-wide association studies (GWASs) have identified thousands of genetic variants associated with agricultural traits. However, due to linkage disequilibrium (LD), disentangling large numbers of linked genetic variants to derive causal effects remains challenging even in species with low LD, such as Zea mays (maize). Maize trait-associated variants are mostly non-genic, and lie ~16.4 kb from the nearest gene, complicating efforts to infer the molecular mechanisms underlying phenotypic diversity. Thus, complementary approaches are required to augment GWAS results and pinpoint causal variants. Gene expression and complex phenotypes are determined by the activity of cis-regulatory elements. However, an understanding of how extant genetic variants affect cis-regulatory activity remains limited. Here, we investigated the consequences of cis-regulatory diversity using single-cell genomics of >0.7 million nuclei across 172 maize inbreds. Our analyses pinpointed cis-regulatory elements distinct to domesticated maize and how transposons rewired the regulatory landscape. We found widespread chromatin accessibility variation associated with >4.6 million genetic variants with largely cell-type-specific effects. Variants in TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR binding sites were the most prevalent determinants of chromatin accessibility. Finally, integration of genetic variants associated with chromatin accessibility, organismal trait variation, and population differentiation revealed how local adaptation has rewired regulatory networks in unique cellular context to alter maize flowering phenotypes.