Working memory is a cornerstone of human cognitive activities, including decision-making and executive control. Understanding whether working memory-related cortical areas are shaped by genetic or environmental factors remains a challenging question. In this study, we analysed functional MRI data from an extensive cohort (n = 424) of monozygotic (MZ) and dizygotic (DZ) twins from the Human Connectome Project dataset to identify working memory-related areas and assess their genetic influence. Activation patterns in these areas were more similar in MZ twins than in DZ twins, highlighting a significant genetic contribution. Working memory-related regions with notable genetic influence included the Medial Intraparietal Area (MIP) in the superior parietal lobule, Area PF and PFm in the inferior parietal lobule, the Primary Motor Cortex in the precentral gyrus, area 2 in the postcentral gyrus, area 6 anterior in the premotor cortex, the Anterior Intraparietal Area (AIP) in the intraparietal sulcus, Intraparietal 1 (IP1) in the intraparietal sulcus, Area PGi and PGs in the angular gyrus, Area IFSa in the inferior frontal sulcus, Parieto-Occipital Sulcus Area 2, posterior 9-46v (p9-46v) in the dorsolateral prefrontal cortex, and the Supplementary and Cingulate Eye Field (SCEF) in the medial frontal cortex. Interestingly, the genetic effects on structural properties followed a distinct pattern, with stronger influences observed in the posterior cingulate cortex, visual cortex, medial temporal cortex, temporo-parieto-occipital junction, insular cortex, somatosensory cortex, and motor cortex. Structural MRI analyses further revealed that genetically influenced voxels were predominantly located in regions with higher cortical curvature in the R-p9-46v area. Moreover, cortex thickness and myelination varied significantly in genetically selected voxels: the cortex was thicker in the selected voxels of the R-7Pm area, thinner in R-AIP areas, and showed higher myelination in selected voxels of the R-7Pm area compared to the rest of voxels. These findings demonstrate that genetic influences on working memory activation patterns are not directly linked to the heritability of macroscopic structural features, providing new insights into the distinct genetic contributions to functional and structural brain characteristics.