Cold-Water Corals (CWCs), and most marine calcifiers, are especially threatened by ocean acidification (OA) and the decrease in the carbonate saturation state of seawater. The vulnerability of these organisms, however, also involves other global stressors like warming, deoxygenation or changes in sea surface productivity and, hence, food supply via the downward transport of organic matter to the deep ocean. This study examined the response of the CWC Desmophyllum dianthus to low pH under different feeding regimes through a long-term incubation experiment. For this experiment, 152 polyps were incubated at pH 8.1, 7.8, 7.5 and 7.2 and two feeding regimes for 14 months. Mean calcification rates over the entire duration of the experiment ranged between −0.3 and 0.3 mg CaCO3 g−1d−1. Polyps incubated at pH 7.2 were the most affected and 30% mortality was observed in this treatment. In addition, many of the surviving polyps at pH 7.2 showed negative calcification rates indicating that, in the long term, CWCs may have difficulty thriving in such aragonite undersaturated waters. The feeding regime had a significant effect on skeletal growth of corals, with high feeding frequency resulting in more positive and variable calcification rates. This was especially evident in corals reared at pH 7.5 (ΩA = 0.8) compared to the low frequency feeding treatment. Early life-stages, which are essential for the recruitment and maintenance of coral communities and their associated biodiversity, were revealed to be at highest risk. Overall, this study demonstrates the vulnerability of D. dianthus corals to low pH and low food availability. Future projected pH decreases and related changes in zooplankton communities may potentially compromise the viability of CWC populations.