Current vaccine strategies against HCMV have focussed on the use or induction of neutralising antibodies targeting entry glycoproteins.  However, clinical trial data suggest these alone may be insufficient, likely due to cell-cell viral transmission, which resists neutralisation. Beyond neutralising cell-free virions, antibodies can bind infected cell surface antigens and activate cellular immunity, including NK cells (antibody-dependent cellular cytotoxicity; ADCC) and macrophages (antibody-dependent cellular phagocytosis; ADCP), enabling control of cell-associated virus. We previously mapped and identified novel viral proteins that were highly effective at promoting ADCC. Here, we asked which antigens drove effective anti-HCMV ADCP. Analysis of serums from a vaccine trial demonstrated that antibodies targeting entry glycoproteins were poor at inducing ADCP. Timecourse analysis indicated that ADCP was maximal at early times (48h) post-infection, prior to the expression of entry glycoproteins and/or virion production. Of 13 viral cell surface antigens expressed at 48h, nine promoted ADCP in isolation; only three also promoted ADCC. However, monoclonal antibodies (mAbs) targeting ADCC-capable antigens failed to induce ADCP against HCMV-infected cells. Although Fc-modifications enabled mAbs to activate ADCC against single antigens, even ADCP-enhancing modifications did not induce ADCP when targeting individual viral proteins. Further analysis revealed that antigen combinations were necessary to achieve ADCP levels comparable to natural infection. These findings demonstrate that ADCC and ADCP rely on distinct antigenic profiles and highlight multiple novel antigens that may need to be included in future vaccines to effectively trigger both responses against HCMV.