Facioscapulohumeral muscular dystrophy (FSHD) is a muscle-wasting disease caused by dysregulation of the D4Z4 macrosatellite array on chromosome 4q, either by repeat contraction (FSHD1) or by mutations in chromatin modifiers such as SMCHD1 (FSHD2). The highly polymorphic tandem repeat structure of the D4Z4 locus, as well as the presence of a homologous D4Z4 array at chromosome 10q, poses challenges for genomic analysis. In our study, we use long-read Cas9 and whole-genome nanopore sequencing to resolve the 4q and 10q alleles for a number of patient samples, including those affected by FSHD1, FSHD2, and another human disease caused by mutations in SMCHD1, Bosma arhinia microphthalmia syndrome (BAMS). We find striking DNA methylation patterns that vary by array length and disease phenotype, demonstrating the potential for improved diagnostics and helping to elucidate the genetic and epigenetic regulation of the D4Z4 locus.