Corals harbour highly diverse microbiomes. However, at present our knowledge on the compartmentalization of coral microbiomes is highly skewed towards the millimetre-thin coral tissue, leaving the diverse coral skeleton microbiome and its functional potential underexplored. Here, we present a genome-centric view of the skeletal microbiome of the reef-building corals' Porites lutea and Isopora palifera, through a compendium of ~400 high-quality archaeal and bacterial metagenome-assembled genomes (MAGs), spanning 34 phyla and 57 microbial classes. Skeletal microbiomes harboured a diverse array of stress response genes, including dimethylsulfoniopropionate synthesis (dsyB) and metabolism (DMSP lyase). Furthermore, skeletal MAGs encoded an average of 22±15 genes in P. lutea and 28±23 in I. palifera with eukaryotic-like motifs thought to be involved in maintaining host association. We provide comprehensive insights into the putative functional role of the skeletal microbiome in key metabolic processes such as nitrogen fixation, dissimilatory and assimilatory nitrate, and sulphate reduction. In summary, we provide critical genomic resources for a better understanding of the coral skeletal microbiome and its role in maintaining coral health, opening new avenues for identifying coral health-beneficial microbes to protect future coral reefs from effects of climate change.