Summary Our knowledge of how the parental genomes interact to shape hybrid performance remains limited. This work established four hybrid maize populations and evaluated plant height (PH) in both the parental and hybrid populations, generating an extensive transcriptome and translatome dataset. We conducted a genome‐wide association study, expression quantitative trait locus (eQTLs) mapping, transcriptome‐wide association mapping (TWAS), and allele‐specific expression analysis to elucidate the regulatory mechanisms underlying PH variation in hybrids. QTLs, eQTLs, and TWAS‐associated genes (TAGs) exhibited both distinct variations and conserved patterns between the maternal and hybrid populations. The functional route (FR)‐following QTLs demonstrated significant nonadditive effects on PH and expression traits. The intergenomic interactions of eQTLs in the heterozygous state drive the nonadditive regulation of eQTL‐regulated genes (eGenes), resulting in the transformation of eGenes into TAGs and eQTLs into nonadditive QTLs for PH. This regulatory mechanism is further supported by the nonadditive regulation of phytohormone‐related genes. Additionally, nonadditive TAGs and QTLs are implicated in regulating nonadditive translation. This study elucidates how nonadditive QTLs contribute to phenotypic variation in hybrid maize, offering a fresh perspective on the understanding of plant heterosis.