Permafrost thaw can stimulate soil carbon release, triggering a positive carbon–climate feedback, which may be mediated by changes in soil phosphorus (P) availability. However, the response of soil P cycling to permafrost thaw and the potential biotic and abiotic mechanisms involved are largely unknown. We investigate how soil P cycling responds to abrupt permafrost thaw based on large-scale sampling along a permafrost transect on the Tibetan Plateau, combined with 31P-nuclear magnetic resonance spectroscopy, 33P-labelling and metagenomic sequencing. In collapsed areas, gross phosphate (Pi) mobilization in the topsoil (0–15 cm) is 50% faster compared with non-collapsed landforms, linked to a higher abundance of microbial P-cycling genes. Meanwhile, plant P uptake increases by 71% due to the enhanced gross Pi mobilization, improved plant P-acquisition capabilities and reduced microbial competition with plants upon permafrost collapse. These findings demonstrate that abrupt permafrost thaw accelerates soil P cycling, which could then mediate the permafrost carbon–climate feedback.