The relationship between intelligence and handedness remains a matter of debate. The present study is a systematic review of 36 studies (totaling 66,108 individuals), which have measured full IQ scores in different handedness groups. Eighteen of those studies were further included in three sets of meta-analyses (totaling 20,442 individuals), which investigated differences in standardized mean IQ scores in (i) left-handers, (ii) non-right-handers, and (iii) mixed-handers compared to right-handers. The bulk of the studies included in the systematic review reported no differences in IQ scores between left- and right-handers. In the meta-analyses, statistically significant differences in mean IQ scores were detected between right-handers and left-handers, but were marginal in magnitude (d = −0.07); the data sets were found to be homogeneous. Significance was lost when the largest study was excluded. No differences in mean IQ scores were found between right-handers and non-right-handers as well as between right-handers and mixed-handers. No sex differences were found. Overall, the intelligence differences between handedness groups in the general population are negligible.