Sponges (phylum Porifera) host complex communities of microbial symbionts that are known to be a rich source of novel secondary metabolites. The symbiotic microbes are generally identified from the sponge extracellular matrix. However, knowledge of intracellular sponge microbiota is scarce. This study hypothesizes that unique microbiomes exist within sponge cells and may provide specific biosynthetic potential. To uncover the endosymbiotic microbiomes, we purified sponge stem cells of Euryspongia arenaria to enrich the intracellular microbes. The intracellular bacterial community of the sponge was initially investigated by 16S rRNA gene amplicon sequencing, which indicated that it hosts three unique phyla not found in the extracellular and bulk tissue microbiomes. The shotgun metagenomic analysis extended the taxonomic coverage to viruses and eukaryotes, revealing the most abundant signature taxa specific to the intracellular microbiome. Functional KEGG pathway annotation showed that the endosymbiotic microbiome hosted the greatest number of unique gene orthologs. The pathway profiles distinguished the intra- and extracellular microbiomes from the tissue and seawater microbiomes. Carbohydrate active enzyme analysis further discriminated each microbiome based on their representative and dominant enzyme families. One pathway involved in digestion system and family esterase had a consistently higher level in the intracellular microbiome and could statistically differentiate the intracellular microbiome from the others, suggesting that triacylglycerol lipases could be the key functional component peculiar to the endosymbionts. The identified higher abundance of lipase-related eggNOG categories further supported the lipid-hydrolysing metabolism of endosymbiotic microbiota. Pseudomonas members, reported as lipase-producing bacteria, were only in the endosymbiotic microbiome. Meanwhile, the genus-level taxa comparison showed a greater abundance of Pseudomonas intracellularly. Our study aided a comprehensive sponge microbiome that demonstrated the taxonomic and functional specificity of endosymbiotic microbiota. The findings not only open the possibility to reveal the low abundant and the likely missed microbiota when directly sequencing the sponge bulk tissues, but also warrant future in-depth exploration within single sponge cells.