An elevated prevalence of atypical handedness (left-, mixed-, or non-right-handedness) has been repeatedly reported in individuals with Autism Spectrum Disorder (ASD) compared to typically developing individuals. However, the exact magnitude of this difference as well as the presence of possible moderating factors remains unknown. Here, we present three sets of meta-analyses of studies that assessed the handedness prevalence among individuals with ASD, totaling 1199 individuals (n = 723 individuals with ASD and n = 476 typically developing individuals). Meta-analysis set 1 found that individuals with ASD are 3.48, 2.49, and 2.34 times more likely to be non-right-handed, left-handed, and mixed-handed compared to typically developing individuals, respectively. Meta-analysis set 2 found a 45.4%, 18.3%, and 36.1% prevalence of non-right-handedness, left-handedness, and mixed-handedness, respectively, amongst individuals with ASD. The classification of handedness, the instrument used to measure handedness, and the main purpose of the study were found to moderate the findings of meta-analysis set 2. Meta-analysis set 3 revealed a trend towards weaker handedness for individuals with ASD. The elevated levels of atypical handedness in individuals with ASD could be attributed to atypicalities in cerebral structure and lateralization for language in individuals with ASD.