Oysters are difficult to classify because of plasticity in shell morphology. Difficulties in classification have hindered the understanding of oyster diversity and evolution. Recent molecular studies of living oysters have revealed high genetic diversity at species, population, and genome levels. New and cryptic species have been discovered, revealing surprisingly high species diversity under similar shell morphology. Genetic analyses have identified several species complexes where low genetic divergence indicates recent or ongoing speciation during the past 3–4 million years. Ongoing speciation is also supported by exceptionally high population divergence within some species. The oyster genome is highly polymorphic and gene-rich, with extensive expansion of genes related to stress and immune responses. High levels of genetic diversity and gene expansion in oysters are likely adaptations to variable environments. Local adaptation in oysters may be pervasive but countered by strong gene flow and balancing or multidirectional selections that favor diversity. Oysters have experienced several expansion and contraction events because of climate change since their origin in Permian. Studies on molecular adaptations to recent and historic climate change may provide insights into the evolution and speciation of oysters.