Larval sea urchins have served as a fundamental system for understanding development, phenotypic plasticity, and life-history evolution over much of the last century. In the recent decade, this understanding has begun to extend to the microbiota associated with larval sea urchins. This dissertation highlights the communities of bacterial symbionts that associate echinoid larvae and how they relate to the ecology and evolution of larval feeding. In particular, larvae acclimate to food-restricted environments by elongating their feeding apparatus to increase their feeding capacity. Chapter 1 of this dissertation shows that expression of this alternative phenotype is correlated with shifts in the bacterial community associated with larval sea urchins and that this response is induced by the environment. Chapter 2 then defines the temporal progression of the larval host and the associated microbiota towards a phenotype-specific bacterial community. Daily profiling of these responses shows that larval urchins follow a four-stage progression and that shifts in the bacterial taxa precede morphological plasticity, suggesting a temporal asynchrony in distinct acclimation responses by larval sea urchins. Chapter 3 then compares these responses between three sea urchin populations from different ocean gyres, showing that despite significant differences in bacterial community structure within each population based on food availability, development, phenotype, and time, variation the bacterial taxa correlated more strongly with geographic location. Lastly, Chapter 4 then shows that these coordinated shifts in larval phenotype and the bacterial symbionts are lost during the major life-history transition from planktotrophy (feeding) to lecithotrophy (non-feeding). In this transition we also find that eggs from the lecithotrophy are dominated by a novel bacterial lineage with close relatives known to manipulate host reproduction. Collectively, this dissertation suggests that the bacterial communities associated with larval sea urchins are integral to their biology and ecology.