IntroductionHandedness is a conspicuous characteristic in human behavior, with a worldwide proportion of approximately 90% of people preferring to use the right hand for many tasks. In the Korean population, the proportion of left‐handedness is relatively low at approximately 7%–10%, similar to that in other East‐Asian cultures in which the use of the left hand for writing and other public activities has historically been oppressed.MethodsIn this study, we conducted two genome‐wide association studies (GWASs) between right‐handedness and left‐handedness, and between right‐handedness and ambidexterity using logistic regression analyses using a Korean community‐based cohort. We also performed association analyses with previously reported variants and our findings.ResultsA total of 8806 participants were included for analysis, and the results identified 28 left‐handedness‐associated and 15 ambidexterity‐associated loci; of these, two left‐handedness loci (NEIL3 [rs11726465] and SVOPL [rs117495448]) and one ambidexterity locus (PDE8B/WDR41 [rs118077080]) showed near genome‐wide significance. Association analyses with previously reported variants replicated ANKS1B (rs7132513) in left‐handedness and ANKIB1 (rs2040498) in ambidexterity.ConclusionThe variants and positional candidate genes identified and replicated in this study were largely associated with brain development, cerebral asymmetry, neurological processes, and neuropsychiatric diseases in line with previous findings. As the first East‐Asian GWAS related to handedness, these results may provide an intriguing reference for further human neurologic research in the future.