Cyanobacterial symbionts may enable sponges to play a critical role in bentho-pelagic coupling, recycling nutrients at the benthic surface and providing a key requirement for ecosystem function. This is the first study to investigate the depths to which these symbioses are viable and the first record of photosynthetic sponges (i.e. sponges having a symbiotic relationship with photosynthetic cyanobacteria) from mesophotic temperate habitats. Sponges with high levels of photosynthetic cyanobacteria occurred at depths of up to 50 m, medium levels to 75 m and low levels to 150 m off south-western Australia. The proportion of sponges that showed no epifluorescence increased greatly with depth. Cyanobacterial symbionts sequenced from sponges at 40 and 50 m belonged to the genera Synechococcus and Synechocystis. Our results verify that the domain of photosynthetic sponges is not just tropical or shallow water temperate environments. Sponges made up the highest biomass of biota across all the sites we sampled from depths of 30–150 m and we hypothesise that photosynthetic cyanobacterial symbionts may be important in facilitating sponges to dominate habitats at these depths off Australia’s oligotrophic west coast.