The glass sponge Aphrocallistes vastus contributes to the formation of large reefs unique to the Northeast Pacific Ocean. These habitats have tremendous filtration capacity that facilitates flow of carbon between trophic levels. Their sensitivity and resilience to climate change, and thus persistence in the Anthropocene, is unknown. Here we show that ocean acidification and warming, alone and in combination have significant adverse effects on pumping capacity, contribute to irreversible tissue withdrawal, and weaken skeletal strength and stiffness of A. vastus. Within one month sponges exposed to warming (including combined treatment) ceased pumping (50–60%) and exhibited tissue withdrawal (10–25%). Thermal and acidification stress significantly reduced skeletal stiffness, and warming weakened it, potentially curtailing reef formation. Environmental data suggests conditions causing irreversible damage are possible in the field at +0.5 °C above current conditions, indicating that ongoing climate change is a serious and immediate threat to A. vastus, reef dependent communities, and potentially other glass sponges.