Interindividual variation in DNA methylation (DNAm) has been linked to both environmental exposures and phenotypic variation. However, DNAm is generally tissue-specific, making the identification of environmentally sensitive variable DNAm states in disease-relevant tissues a challenge. First discovered in isogenic mice, metastable epialleles (MEs) are DNAm loci that vary between individuals but are correlated across tissues derived from different germ layers within a given individual. This property, termed systemic interindividual variation or ‘SIV’, is attributed to stochastic methylation establishment in the early embryo. In humans, the ME definition can be broadened to include SIV loci that are influenced but not determined by genotype. Human MEs show sensitivity to the periconceptional environment and have been associated with metabolism, cancer, immunity, and neurocognitive function, making them useful for exploring how the environment experienced in early development can influence health outcomes in later life via epigenetic mechanisms using easily accessible tissues. We analysed DNA methylation data from 30 datasets comprising 3,474 individuals, 19 tissues and 8 ethnicities at CpGs covered by the Illumina450K array. We identified 4,143 hypervariable CpGs (‘hvCpGs’) with methylation in the top 5% most variable sites across multiple tissues and ethnicities. hvCpG methylation was influenced but not determined by genetic variation, and was not linked to probe reliability, epigenetic drift, age, sex or cell heterogeneity effects. Instead, hvCpGs overlapped or colocalised with many previously identified MEs, showed unique methylation patterns in monozygotic (MZ) twins, and were enriched for loci previously associated with the periconceptional environment, suggesting that DNAm establishment at many hvCpGs occurs in the early embryo. hvCpGs also showed SIV in foetal tissues at previously unreported MEs, suggesting that the identification of hvCpGs may be a powerful ME detection method compared to existing SIV screens that rely on rare multi-tissue methylation datasets with small sample sizes. Variable methylation at murine MEs has been recently linked to Krüppel-associated box (KRAB) domain proteins (KZFPs), that epigenetically silence transposable elements (TEs) in embryonic stem cells (ESCs) by recruiting KAP1 (KRAB-associated protein-1). By examining hvCpG proximity to retrotransposons, KAP1 binding sites, and associations with genetic variation at KZFP genes in trans, we found evidence that KZFP-mediated silencing of TEs may influence methylation at some hvCpGs. We identified an example of how this mechanism may affect phenotype in later life: a differentially methylated region comprising hvCpGs in the promoter of C8orf31 which is influenced by ZNF808-mediated silencing of the retrotransposon MER11C and shows evidence of a causal effect on pancreatic beta cell function. In summary, our findings: i) position hvCpGs as age-stable biomarkers of early stochastic and/or environmental effects on DNA methylation, useful for exploring the developmental origins of health and disease; and ii) highlight KZFP-mediated silencing of TEs as a novel mechanism by which variable DNAm loci established in the early human embryo can influence phenotype in later life.