N2 fixation by the genus Trichodesmium is predicted to support a large proportion of the primary productivity across the oligotrophic oceans, regions that are considered among the largest biomes on Earth. Many of these environments remain poorly sampled, limiting our understanding of Trichodesmium physiological ecology in these critical oligotrophic regions. Trichodesmium colonies, communities that consisted of the Trichodesmium host and their associated microbiome, were collected across the oligotrophic western tropical South Pacific (WTSP). These samples were used to assess host clade distribution, host and microbiome (holobiont) metabolic potential, and functional gene expression, with a focus on identifying Trichodesmium physiological ecology in this region. Expression dynamics across the WTSP transect indicated potential co-limitation of Trichodesmium for phosphorus and iron. A gene cassette for phosphonate biosynthesis was detected in Trichodesmium, the expression of which co-varied with the abundance of Trichodesmium Clade III, which was unusually abundant relative to Clade I in this environment. Coincident with the expression of the gene cassette, phosphate reduction to phosphite and low molecular weight phosphonate compounds was measured in Trichodesmium colonies as well as genes that enable use of this reduced phosphorus in both Trichodesmium and the microbiome. Overall, these results highlight physiological strategies for survival by the Trichodesmium holobiont in the oligotrophic ocean, revealing mechanisms with the potential to influence the cycling of resources like nitrogen and phosphorus.