Climate change threatens freshwater ecosystems, potentially intensifying cyanobacterial blooms and antibiotic resistance. We investigated these risks in Cosseys Reservoir, New Zealand, using short-term warming simulations (22 °C, 24 °C, and 27 °C) with additional oxidative stress treatments. A metagenomic analysis revealed significant community shifts under warming. The cyanobacterial abundance increased from 6.11% to 20.53% at 24 °C, with Microcystaceae and Nostocaceae proliferating considerably. The microcystin synthesis gene (mcy) cluster showed a strong association with cyanobacterial abundance. Cyanobacteria exhibited enhanced nutrient acquisition (pstS gene) and an upregulated nitrogen metabolism under warming. Concurrently, antibiotic resistance genes (ARGs) increased, particularly multidrug resistance genes (50.82% of total ARGs). A co-association network analysis identified the key antibiotic-resistant bacteria (e.g., Streptococcus pneumoniae and Acinetobacter baylyi) and ARGs (e.g., acrB, MexK, rpoB2, and bacA) central to resistance dissemination under warming conditions. Oxidative stress exacerbated both cyanobacterial growth and ARGs’ proliferation, especially efflux pump genes (e.g., acrB, adeJ, ceoB, emrB, MexK, and muxB). This study demonstrated that even modest warming (2–5 °C) could promote both toxic cyanobacteria and antibiotic resistance. These findings underscore the synergistic effects of temperature and oxidative stress posed by climate change on water quality and public health, emphasizing the need for targeted management strategies in freshwater ecosystems. Future research should focus on long-term impacts and potential mitigation measures.