Tropical coral reefs are highly productive ecosystems thriving in oligotrophic waters, a phenomenon facilitated by efficient but delicate biogeochemical cycling within reef communities. Global climate change and local stressors are driving phase shifts from coral- to non-calcifier-dominated states in reefs worldwide, substantially altering reef biogeochemical functioning. While major benthic players such as coral and macroalgae have been investigated in detail regarding carbon and nutrient dynamics, the less conspicuous “reef cryptobiome” (sensu Carvalho et al., 2019) – comprising most of reef diversity – has only recently gained attention. Autonomous Reef Monitoring Structures (ARMS) have recently been developed to sample coral reef cryptobenthic communities in a non-destructive and standardised way, allowing exploration of these often overlooked biota. Here, 16 ARMS were deployed for seven months in four distinct habitats dominated by different benthic players (i.e., four units per habitat) in a nearshore Red Sea coral reef to investigate the cryptobiome associated with proxies of varying benthic states. Two of these habitats were coral-dominated, and one each dominated by turf algae or coral rubble. To assess the biogeochemical fluxes of pioneering cryptobenthic communities, ARMS were incubated in situ prior to retrieval using customised chambers. Subsequently, 16S rRNA gene amplicon and shotgun metagenomic sequencing of the ARMS sessile (i.e., encrusting) fractions were performed to link observed fluxes with prokaryotic taxonomic and functional profiles, particularly regarding nitrogen cycling. The results show that the pioneering cryptobiome represents a significant source of inorganic nutrients and that its associated microbial communities facilitate the mineralisation and assimilation of organic matter and provide crucial genetic functional pathways for nitrogen cycling. Functional similarities among habitats suggested functional redundancy despite variation in bacterial community composition. Hence, the reef cryptobiome can be considered an important biogeochemical player in coral reefs, actively shaping the abiotic conditions within niches of the reef framework and driving the recruitment and persistence of crytobenthic and other reef organisms. As communities associated with the algae-dominated reef habitat were most distinct compositionally and biogeochemically, and as non-calcifiers are becoming more dominant in many reefs, this has implications for intensifying phase shifts in coral reefs worldwide. Future ARMS studies will also benefit from adjustment of sample processing and molecular protocols, resulting in higher sample throughput and lower costs in times of increased application of ARMS.