Anatomical and functional asymmetries were measured using MRI and dichotic, visual field and hand performance laterality tasks in 104 normal right- and left-handed male and female adults. Comprehensive linear and area measures showed consistently larger brains when handedness and language laterality were in the same direction. Right-handers with left cerebral dominance for dichotic listening and left-handers with right cerebral dominance had larger structures. Hand performance was the strongest functional laterality related to anatomical asymmetries. Left hemisphere dominance on this task was associated with larger right frontal and left occipital widths. Dichotic listening or visual field laterality alone was not associated with contralaterally larger temporal, parietal or occipital measurements. Left visual field dominance for reading, interacting with right-handedness, was associated with wider left parietal width. The complex associations between anatomical and functional asymmetries contribute to individual differences in cerebral organization. The demonstrated association of coincident hand performance and language laterality measures with larger anatomical structures may confer biological advantage. Morphometric analysis in vivo may have increasing importance in interpreting behaviour.