While diagnosing autism spectrum disorder (ASD) based on an objective test is desired, the current diagnostic practice involves observation-based criteria. This study is a systematic review and meta-analysis of studies that aim to diagnose ASD using magnetic resonance imaging (MRI). The main objective is to describe the state of the art of diagnosing ASD using MRI in terms of performance metrics and interpretation. Furthermore, subgroups, including different MRI modalities and statistical heterogeneity, are analyzed. Studies that dichotomously diagnose individuals with ASD and healthy controls by analyses progressing from magnetic resonance imaging obtained in a resting state were systematically selected by two independent reviewers. Studies were sought on Web of Science and PubMed, which were last accessed on February 24, 2023. The included studies were assessed on quality and risk of bias using the revised Quality Assessment of Diagnostic Accuracy Studies tool. A bivariate random-effects model was used for syntheses. One hundred and thirty-four studies were included comprising 159 eligible experiments. Despite the overlap in the studied samples, an estimated 4982 unique participants consisting of 2439 individuals with ASD and 2543 healthy controls were included. The pooled summary estimates of diagnostic performance are 76.0% sensitivity (95% CI 74.1–77.8), 75.7% specificity (95% CI 74.0–77.4), and an area under curve of 0.823, but uncertainty in the study assessments limits confidence. The main limitations are heterogeneity and uncertainty about the generalization of diagnostic performance. Therefore, comparisons between subgroups were considered inappropriate. Despite the current limitations, methods progressing from MRI approach the diagnostic performance needed for clinical practice. The state of the art has obstacles but shows potential for future clinical application.