The opportunistic pathogen Vibrio parahaemolyticus poses a significant food safety risk worldwide, and understanding its growth in commercially cultivated oysters, especially at temperatures likely to be encountered post-harvest, provides essential information to provide the safe supply of oysters. The Blacklip Rock Oyster (BRO) is an emerging commercial species in tropical northern Australia and as a warm water species, it is potentially exposed to Vibrio spp. In order to determine the growth characteristics of Vibrio parahaemolyticus in BRO post-harvest, four V. parahaemolyticus strains isolated from oysters were injected into BROs and the level of V. parahaemolyticus was measured at different time points in oysters stored at four temperatures. Estimated growth rates were −0.001, 0.003, 0.032, and 0.047 log10 CFU/h at 4 °C, 13 °C, 18 °C, and 25 °C, respectively. The highest maximum population density of 5.31 log10 CFU/g was achieved at 18 °C after 116 h. There was no growth of V. parahaemolyticus at 4 °C, slow growth at 13 °C, but notably, growth occurred at 18 °C and 25 °C. Vibrio parahaemolyticus growth at 18 °C and 25 °C was not significantly different from each other but were significantly higher than at 13 °C (polynomial GLM model, interaction terms between time and temperature groups p < 0.05). Results support the safe storage of BROs at both 4 °C and 13 °C. This V. parahaemolyticus growth data will inform regulators and assist the Australian oyster industry to develop guidelines for BRO storage and transport to maximise product quality and safety.