Unicellular, nitrogen-fixing cyanobacteria (UCYN) thrive and support primary production in oligotrophic oceans, playing a significant role in the marine nitrogen cycle. Crocosphaera sp, a model for studying marine nitrogen fixation, is adapted to low phosphate (P i ) conditions. Yet, how Crocosphaera copes with P i depletion is rather poorly understood. We present genomics analysis of P i stress-responsive genes in this genus, encompassing six C. watsonii genomes and two strains isolated in coastal environments, C. subtropica and C. chwakensis . We identified genes involved in P i signaling, uptake, and dissolved organic phosphorus (DOP) hydrolysis. Results showed different genetic potentials to cope with P i scarcity between the Crocosphaera strains. Physiological monitoring of cultures of C. watsonii WH8501 exposed to P i depletion highlighted a capacity to divide several times and survive for a few more days, albeit with a skewed C:N:P stoichiometry. Upon addition of DOP, cultures efficiently recovered to a growth rate and cell composition equivalent to those observed under favorable conditions. The concomitant transcription analysis revealed diel expression patterns of P i -related genes and endogenous clock genes, suggesting a possible circadian regulation. Our data deepen our understanding of the growth strategies Crocosphaera employs in P i -limited environments, offering broader insights into microbial resilience in marine ecosystems.