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Autism Spectrum Disorder (ASD) diagnosis is still based on behavioral criteria through a lengthy and time-consuming process. Much effort is being made to identify brain imaging biomarkers and develop tools that could facilitate its diagnosis. In particular, using Machine Learning classifiers based on resting-state fMRI (rs-fMRI) data is promising, but there is an ongoing need for further research on their accuracy and reliability. Therefore, we conducted a systematic review and meta-analysis to summarize the available evidence in the literature so far. A bivariate random-effects meta-analytic model was implemented to investigate the sensitivity and specificity across the 55 studies that offered sufficient information for quantitative analysis. Our results indicated overall summary sensitivity and specificity estimates of 73.8% and 74.8%, respectively. SVM stood out as the most used classifier, presenting summary estimates above 76%. Studies with bigger samples tended to obtain worse accuracies, except in the subgroup analysis for ANN classifiers. The use of other brain imaging or phenotypic data to complement rs-fMRI information seems promising, achieving higher sensitivities when compared to rs-fMRI data alone (84.7% versus 72.8%). Finally, our analysis showed AUC values between acceptable and excellent. Still, given the many limitations indicated in our study, further well-designed studies are warranted to extend the potential use of those classification algorithms to clinical settings.