The genetic diversity of a population defines its ability to adapt to episodic and fluctuating environmental changes. For species of agricultural value, available genetic diversity also determines their breeding potential. Comprehensive knowledge of the extant gene pool in Pacific oysters (Magallana gigas, previously Crassostrea gigas) remains fundamental to the development of practices that maintain health and productivity in this species. In this study we use whole genome resequencing to evaluate the genetic diversity within and between naturalized and captively reared Pacific oyster populations from in the US Pacific coast. The analyses included individuals from preserved samples dating to 1998 (Dabob Bay; a.k.a. MBP6) and 2004 (Midori). Two contemporary naturalized populations (Willapa Bay and San Diego Bay), and one domesticated population (MBP30) were also included. We show that despite high overall heterozygosity, there was extremely low genetic divergence between populations. The MBP30 population which was reared in captivity for over 25 years was the most genetically distinct population and exhibited reduced nucleotide diversity, attributable to inbreeding. Fifty-nine significant FST outlier sites were identified, the majority of which were individually present in high proportions of the MBP30 samples, and which are possibly associated with domestication. Our results show that Pacific oysters in the US Pacific coast may hold enough genetic diversity to sustain health and efficient commercial productivity, but captive populations need to be actively managed to prevent inbreeding depression.