Heterotrophic bacteria are central players in the ocean’s carbon and nutrient cycles, shaping marine ecosystems through their diverse metabolic and ecological functions. This dissertation identifies abiotic and biotic factors that shape bacterial activities and form the dimensions of their niche, a foundational ecological concept to explain the distribution of species in natural environments. Here, the niche dimensions of marine bacteria associated with phytoplankton were addressed through analysis of microbial genes, transcripts, and genomes in dynamic coastal waters. In the first study, diversity and temporal dynamics of genes encoding bacterial transformation of an important resource dimension, the abundant phytoplankton- derived osmolyte dimethylsulfoniopropionate (DMSP), were measured in surface waters of Monterey Bay, CA. Shifts in abundance of paralogous genes that encode production of the volatile sulfur gas dimethylsulfide from DMSP occurred as bacterial communities responded to environmental conditions. Positive relationships between abundance of DMSP-producing dinoflagellates and specific bacterial taxa emerged. In the second study, a time-series dataset of metagenomes, metatranscriptomes, and 16S and 18S rRNA gene libraries over 52 days of a massive dinoflagellate bloom in Monterey Bay is reported. This comprehensive sequence dataset and accompanying measures of chemical and biological conditions will facilitate studies of the metabolic responses of heterotrophic bacteria during episodic phytoplankton blooms. In the third study, niche dimensions of a well-characterized heterotrophic marine bacterium, Ruegeria pomeroyi, were explored by conducting serial invasions of this model bacterium into Monterey Bay bloom seawater and assessing transcriptome composition and apparent growth rates. Differential gene expression patterns indicated relevant substrate, vitamin, nutrient, metal, stress, and biotic interaction factors serving as key niche dimensions in this environment. In the fourth study, genomes were assembled from bloom seawater communities to provide insights into the ecological capabilities of dominant taxa in the natural bacterioplankton community. This revealed two highly related, sequence-discrete species from the roseobacter group that dominated the bacterial community during the bloom. From metapangenomic analysis of 31 genomes from these species, genes involving substrate transformation (polyamines, urea, sugars, sulfur, and carboxylic acids), metal dynamics, vitamin synthesis, and phototrophy provided insights into the dimensions of niche overlap and differentiation in these sympatric species.