Single Molecule Real Time (SMRT) sequencing represents a long-read methodology capable of decoding individual molecules and performing real-time detection of their methylation status, which makes it an approach with the potential for fully characterizing expanded CGG repeats within the FMR1 gene. In this analysis, we use SMRT sequencing to interrogate the CGG repeat lengths and associated methylation profiles of molecules enriched from completely unmethylated and methylated plasmids, and three genomic samples with expanded CGG repeat alleles. The experimental design was to use the plasmid molecules as controls to predict the methylation status of genomic molecules, with the goal to detect inter- and intra-molecular variation in the expanded genomic CGG repeats. We find that not only is methylation particularly difficult to quantify from SMRT sequencing output, but there are also pronounced strand-specific effects on estimates of methylation status that complicate biological interpretation. Despite these challenges, we identify significant intermolecular variation in methylation profiles that support clinical evidence of methylation mosaicism in patient populations. Future analyses producing higher coverage of CGG molecules may be able to further our understanding of the association of CGG repeat length and methylation patterning, especially how these molecular signatures relate to clinical phenotypes outcomes.