Epigenetics is an emerging area of investigation for Autism Spectrum Disorder (ASD). Integration of epigenetic information with ASD genetic results may elucidate functional insights not possible via either source of information in isolation. We used concurrent genotype and DNA methylation (DNAm) data from cord blood and peripheral blood from preschool-aged children to identify SNPs associated with DNA methylation, or methylation quantitative trait loci (meQTLs), and combined this with publicly available fetal brain and lung meQTL lists to assess enrichment of ASD GWAS results for tissue-specific meQTLs. ASD-associated SNPs were enriched for fetal brain (OR = 3.55; p < 0.001) and peripheral blood meQTLs (OR = 1.58; p < 0.001). The CpG site targets of ASD meQTLs across cord, blood, and brain tissues were enriched for immune-related pathways, consistent with other expression and DNAm results in ASD, and revealing pathways not implicated by genes identified from ASD rare variant work. Further, DNaseI hypersensitive sites and the STAT1 and TAF1 transcription factor binding sites were enriched for meQTL target CpGs of SNPs associated with psychiatric conditions. This joint analysis of genotype and DNAm demonstrates the potential utility of both brain and blood-based DNAm for insights into ASD and psychiatric phenotypes more broadly.