Sponges can harbour diverse communities of microbial symbionts, collectively referred to as a holobiont. Sponge symbionts play important ecological and mutualistic roles, including cycling of carbon, nitrogen, and sulfur; provisioning the host with essential compounds; and producing bioactive metabolites that confer fitness advantages to the holobiont. Recent metagenomics and bioinformatics advances facilitate genomic reconstruction and metabolic characterisation of uncultured prokaryotic species. Leveraging these tools, I reconstructed 75 metagenome-assembled genomes (MAGs) that represent 21 novel sponge-associated species: ten Gammaproteobacteria, six Acidimicrobiia, and five Acidobacteriota. The gammaproteobacterial species were metabolically diverse, likely representing adaptations to diverse habitats associated with different sponge species. Two species from the Candidatus genus Azotimanducus comprised almost identical patterns of organoheterotrophy that likely enabled them to colonize the same sponge host, but differed in other features that likely allowed for niche partitioning and cohabitation. Unlike the sponge-associated Gammaproteobacteria, the Acidimicrobiia shared very similar genomic features. Of particular interest, sponge-associated Acidimicrobiia were predicted to produce bioactive compounds that may modulate host signalling pathways, suggesting a potential role in host health. The sponge-associated Acidobacteriota likely predominantly formed symbiosis with their hosts prior to the phylogenetic split between sponges and corals. All five acidobacteriotal species shared similar patterns of organoheterotrophy, likely allowing for scavenging organic substrates from the host environment. Another feature that was specifically enriched in the novel sponge-associated Acidobacteriota was their capacity to produce diverse B-vitamins, with Candidatus Versatilivorator vitaminiformans comprising the genetic capacity to produce all of them. All 21 novel species also comprised unique respiratory, degradation, biosynthetic, and defensive features that likely mediate their interactions with the corresponding hosts. Features shared by the majority of the species were also identified. Altogether, the comprehensive genomic characterisation of sponge symbionts in this thesis has uncovered unique and shared features, highlighting the importance of extensive surveys into uncultured sponge symbiont diversity and function.