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We investigated intra- and inter-colony sequence variation in a population of the dominant Hawaiian coral Montipora capitata by analyzing marker gene and genomic data. Ribosomal ITS1 regions showed evidence of a reticulate history among the colonies, suggesting incomplete rDNA repeat homogenization. Analysis of the mitochondrial genome identified a major (M. capitata) and a minor (M. flabellata) haplotype in single polyp-derived sperm bundle DNA with some colonies containing 2–3 different mtDNA haplotypes. In contrast, Pax-C and newly identified single-copy nuclear genes showed either no sequence differences or minor variations in SNP frequencies segregating among the colonies. Our data suggest past mitochondrial introgression in M. capitata, whereas nuclear single-copy loci show limited variation, highlighting the divergent evolutionary histories of these coral DNA markers.