Sturgeon aquaculture faces challenges due to global warming, as chronic heat stress (CHS) jeopardises fish health and production sustainability. To tackle this issue, we analysed serum innate components and the cellular composition of the peritoneum in Russian sturgeons (Acipenser gueldenstaedtii) subjected to CHS and challenged with Aeromonas hydrophila. Russian sturgeons exposed to CHS exhibited a reduction in the serum levels of total protein and alkaline phosphatase activity, trending to a higher decrease in sturgeons exposed to both bacterial challenge and CHS. This sturgeon group showed a worsened health status, reduced growth and a higher mortality rate. Under tolerable temperatures, the bacterial challenge increased serum ceruloplasmin, lysozyme and serum amyloid A levels, which tended to be lower under CHS. The naive peritoneal cellular composition of the Russian sturgeon revealed a predominance of myeloid cells, with lymphoid cells present in a smaller proportion. CHS altered this distribution, increasing lymphoid while reducing myeloid cell percentages and A. hydrophila challenge reverted these alterations. Myeloid cells exhibiting the highest phagocytic potential were reduced by CHS, potentially compromising peritoneal bacterial clearance. Principal component analysis revealed that sturgeons' integral innate response varied according to temperature exposure, evidencing CHS's impact on the anti-bacterial response. Overall, this study provides a first picture of the peritoneal cellular composition of a chondrostean fish. Furthermore, it demonstrates the disruption caused by CHS on the sturgeon's early systemic and peritoneal responses mounted against A. hydrophila.