Meta-analyses have shown that several neurodevelopmental and psychiatric disorders, such as autism spectrum disorder and schizophrenia, are associated with a higher prevalence of atypical (left-, non-right-, and/or mixed-) handedness. One neurodevelopmental disorder for which this association is unclear is attention deficit hyperactivity disorder (ADHD). Here, some empirical studies have found evidence for a higher prevalence of atypical handedness in individuals with ADHD compared to neurotypical individuals. However, other studies failed to establish such an association. Therefore, meta-analytic integration is critical to estimate whether or not there is an association between handedness and ADHD. We report the results of three meta-analyses (left-, mixed-, and non-right-handedness) comparing handedness in individuals with ADHD to controls (typically developing individuals). The results show evidence of a trend towards elevated levels of atypical handedness when it comes to differences in left- and mixed-handedness (p = 0.09 and p = 0.07, respectively), but do show clear evidence of elevated levels of non-right-handedness between individuals with ADHD and controls (p = 0.02). These findings are discussed in the context of the hypothesis that ADHD is a disorder in which mostly right-hemispheric brain networks are affected. Since right-handedness represents a dominance of the left motor cortex for fine motor behavior, such as writing, as well as a left-hemispheric dominance for language functions, and about 90% of individuals are right-handers, this hypothesis might explain why there is not stronger evidence for an association of left-handedness with ADHD. We suggest that the mechanisms involved in the pathogenesis of ADHD might show an overlap with the mechanisms involved in handedness strength, but not handedness direction.