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11 pages, 5 figures, 1 table, supplementary information https://doi.org/10.1038/s41396-021-00900-6 ; Bacteriophages (phages) are ubiquitous elements in nature, but their ecology and role in animals remains little understood. Sponges represent the oldest known extant animal-microbe symbiosis and are associated with dense and diverse microbial consortia. Here we investigate the tripartite interaction between phages, bacterial symbionts, and the sponge host. We combined imaging and bioinformatics to tackle important questions on who the phage hosts are and what the replication mode and spatial distribution within the animal is. This approach led to the discovery of distinct phage-microbe infection networks in sponge versus seawater microbiomes. A new correlative in situ imaging approach ('PhageFISH-CLEM') localised phages within bacterial symbiont cells, but also within phagocytotically active sponge cells. We postulate that the phagocytosis of free virions by sponge cells modulates phage-bacteria ratios and ultimately controls infection dynamics. Prediction of phage replication strategies indicated a distinct pattern, where lysogeny dominates the sponge microbiome, likely fostered by sponge host-mediated virion clearance, while lysis dominates in seawater. Collectively, this work provides new insights into phage ecology within sponges, highlighting the importance of tripartite animal-phage-bacterium interplay in holobiont functioning. We anticipate that our imaging approach will be instrumental to further understanding of viral distribution and cellular association in animal hosts ; We acknowledge funding by the DFG CRC1182 to UH (TPC4.3), TL (TPC4.2). MTJ was supported by a grant of the German Excellence Initiative to the Graduate School of Life Sciences, University of Wuerzburg, and a Young Investigator Award of the CRC1182. SMM was supported by the Studienstiftung des Deutschen Volkes (German Academic Scholarship Foundation). CS was supported by the grants DFG STI700/1-1 and GRK2581 (P6). MR was supported by the Spanish Government grant (RTI2018-094187-B100) and 'Generalitat de Catalunya' research group grant (2017SGR1011). BED was supported by the Netherlands Organisation for Scientific Research (NWO) Vidi grant 864.14.004 and by the European Research Council (ERC) Consolidator grant 865694: DiversiPHI. /./ Open Access funding enabled and organized by Projekt DEA ; With the funding support of the 'Severo Ochoa Centre of Excellence' accreditation (CEX2019-000928-S), of the Spanish Research Agency (AEI) ; Peer reviewed