Background: Triploidy can occur in many animal species but is often lethal. Among invertebrates, amphibians and fishes, triploids are viable although often sterile or infertile. Most triploids of the Pacific oyster Crassostrea gigas are almost sterile (named "3n beta'') yet a low but significant proportion show an advanced gametogenesis (named "3n alpha''). These oysters thus constitute an interesting model to study the effect of triploidy on germ cell development. We used microarrays to compare the gonad transcriptomes of diploid 2n and the abovementioned triploid 3n beta and 3n alpha male and female oysters throughout gametogenesis. Results: All triploids displayed an upregulation of genes related to DNA repair and apoptosis and a downregulation of genes associated with cell division. The comparison of 3n alpha and 3n beta transcriptomes with 2n revealed the likely involvement of a cell cycle checkpoint during mitosis in the successful but delayed development of gonads in 3n alpha individuals. In contrast, a disruption of sex differentiation mechanisms may explain the sterility of 3n beta individuals with 3n beta females expressing male-specific genes and 3n beta males expressing female-specific genes. Conclusions: The disruption of sex differentiation and mitosis may be responsible for the impaired gametogenesis of triploid Pacific oysters. The function of the numerous candidate genes identified in our study should now be studied in detail in order to elucidate their role in sex determination, mitosis/meiosis control, pachytene cell cycle checkpoint, and the control of DNA repair/apoptosis.