Microbial communities dominate the oceans, forming 70–90% of biomass and driving Earth-system processes. Surface microbes generate ~46% of primary production and support CO₂ sequestration, yet these processes are constrained by low inorganic phosphate, often below uptake thresholds (<10 nM). In phosphate-depleted regions, phosphonates can sustain ~25% of primary production. As climate-driven stratification restricts nutrient fluxes, reliance on phosphonates will increase, although pathways and regulatory mechanisms enabling utilisation are poorly resolved. We coupled in-silico and in-vivo experiments to investigate organophosphonate cycling across the global oceans and assessed their importance relative to other phosphorus-acquisition pathways across basins, depths, and nutrient gradients. Several genes and transcripts increased with vertical stratification and rising inorganic-phosphate, suggesting regulation beyond simple phosphorus-limitation. Notably, phnJ, the key methylphosphonate-degrading and methane-releasing gene, was enriched in phosphate-depleted regions, indicating selection under phosphorus-limitation. Proteobacteria dominated global organophosphonate-utilising communities. To validate these patterns, we conducted growth assays and cell-free lysate experiments in the marine Alpharoteobacterium Roseovarius nubinhibens. We identified phosphonate catabolism genes, including phnWYA, clustered with the novel pbfA gene and C-P lyase. R. nubinhibens utilizes various phosphonates, such as 2-aminoethylphosphonate, R-1-hydroxy-2-aminoethylphosphonate, and methylphosphonate, as phosphorus sources.  Functional assays showed that R. nubinhibens can funnel R-1-hydroxy-2-aminoethylphosphonate into a catabolic route previously thought to be specific for 2-aminoethylphosphonate following a novel variation of the pathway, PbfA-PhnYA and thus expanding metabolic versatility. Aminophosphonate metabolism was substrate-inducible and LysR-regulated, providing the first evidence of this pathway and its phosphate-independent regulation. Together, these findings reveal significant metabolic flexibility in phosphonate utilisation under changing ocean conditions.