Genomic variation in stony corals remains poorly understood with population genetic data implicating processes such as chimerism and genetic mosaicism in colony evolution. Here we asked whether coral genetic architecture supports this view of divergent DNA composition. We determined the extent of intra and inter-colony sequence variation by studying gene and genomic data from Montipora capitata reefs in Kaneohe Bay, Hawai’i. Ribosomal ITS1 and mitochondrial control region (MTC) sequences were initially characterized, followed by analysis of genome and transcriptome data from individual sperm bundle (single polyp) and pooled sperm bundle (colony) extracts. ITS1 data from three colonies across two reefs supported M. capitata monophyly but these diverged sequences had a reticulate history, suggesting incomplete rDNA repeat homogenization. The MTC data identified a major and a minor haplotype in single sperm bundle DNA and supported M. capitata polyphyly with the three colonies each containing 2-3 haplotypes. In contrast, analysis of nine single-copy nuclear genes and genomic data from single and multiple sperm bundle extracts from 3 colonies and the Pax-C intron sequence from an additional two colonies in three reefs showed either no sequence differences or minor variations in SNP frequencies segregating in these colonies, excluding chimerism in these samples. Our results provide the first genome-wide insights into coral colony genetic structure in a local population of M. capitata. We demonstrate the importance of choosing the appropriate marker for studying coral phylogeography, with ITS1 and MTC providing poorly resolved or conflicting data when compared to nuclear single-copy coding regions.