The Pacific Oyster (Crassostrea gigas) is one of the most economically and ecologically significant shellfish species worldwide. In the Pacific Northwest United States (PNW), the sustainability oyster stocks is increasingly threatened by ocean acidification (OA), which has had significant negative effects on the aquaculture industry in this region over the last decade. Currently, little is known with regards to stock-based differences in larval fitness for PNW populations of C. gigas in ambient or high pCO2 conditions. Furthermore, no studies have been performed that evaluate the genetic consequences of larval rearing in acidified seawater for Pacific oysters. Here I examined genetic components of larval fitness traits, both in ambient seawater as well as simulated OA conditions. In Chapter 2 my co-authors and I conducted two experiments to compare the relative fitness of larvae from selectively bred aquaculture stocks to those spawned from a naturalized source of broodstock in Willapa Bay, WA. We reared genetically diverse pools of larvae from each group in ambient (~400 μatm) and high (~1600 μatm) pCO2 seawater for 22-24 days from fertilization through settlement to juvenile stage. Overall, we found that the impacts of high pCO2 seawater on larval phenotypes were heterogeneous across larval developmental stages and variable between the two experiments. Nevertheless, larvae from selectively bred lines had consistently higher survival and greater developmental success through settlement than those from naturalized stocks across both conditions and experiments. In Chapter 3 we analyzed the overall changes in genetic composition of each larval pool created in the first experiment. We found an abundance of loci with significantly distorted allele frequencies across larval development, nearly all of which were specific to each broodstock type. There were additional genetic changes owing to high pCO2 culture that, also, were largely unique to each parental group. Overall, larvae from selectively bred stocks had significantly less genetic change than those from naturalized populations, both for general larval development as well as survival in acidified seawater. We performed functional enrichment analyses on genes associated with distorted loci and found that those with altered allele frequencies in acidified seawater were significantly over-represented by gene-ontology categories concerning membrane structure and function. This finding is consistent with previous studies which also highlighted this aspect of larval physiology as a critical component for survival in acidified conditions. The reduced genetic change in larvae from selected lines suggests that multiple generations of hatchery culture has had a domesticating effect on the genotypes of selectively bred oyster stocks. These results also support the phenotypic results from Chapter 2 which suggested that general improvements to larval fitness have crossover benefits for environmental stressors like OA. In Chapter 4 we further investigated the dynamic genetic changes taking place in larval populations during development, absent any overt environmental stress. By analyzing temporal patterns of changes in allele frequencies across development, we observed that genetic changes were highly dynamic, with more than a quarter that displayed significant shifts in allele frequencies changing in direction across developmental transitions. Importantly, this resulted in the detection of substantially more genetic changes taking place than were indicated from overall analyses from ‘start’ and ‘end’ points in larval culture examined in Chapter 3. These findings represent a novel and unparalleled analysis of the genetic impacts of genotype-dependent mortality in oysters. The patterns of viability selection that we describe likely have extensive consequences on the genetic diversity of this species, and its long term capacity for adaptation.