With the emergence of Middle East respiratory syndrome coronavirus (MERS-CoV) and the recently-discovered HKU5-CoV-2, the threat of merbecoviruses is increasingly relevant. Currently, no broadly neutralising monoclonal antibodies exist for merbecoviruses, highlighting a critical gap in pandemic preparedness. This could be attributed to current antibody screening approaches which mainly select antibody candidates based on binding efficacy, which may not directly translate into viral neutralisation. To bridge the gap, we adapted the surrogate virus neutralisation test (sVNT) format into a high-throughput screening platform capable of directly identifying antibodies capable of blocking the MERS-CoV receptor-binding domain (MERS-RBD) engagement with its host receptor, dipeptidyl peptidase 4 (DPP4). The single-cell sVNT (sc-sVNT) works by first compartmentalising individual antibody-secreting cells and MERS-RBD-functionalized particles into more than 1,000,000 picoliter-sized hydrogel beads. Subsequently, neutralizing antibodies can then be identified by identifying antibody candidates that inhibit a fluorescently labelled wildtype DPP4 to the MERS-RBD particles. We foresee the sc-sVNT as a useful tool in the discovery of broadly neutralising monoclonal antibodies, advancing therapeutics against MERS-CoV and emerging merbecoviruses.