Eukaryotic proteins are often targets of posttranslational modifications (PTMs). Capsid protein (CP) of plum pox virus (PPV), a member of genus Potyvirus, has been reported to be prone to phosphorylation in four serines at the N-terminal region. CP phosphorylation has been proposed to influence PPV infection by regulating CP accumulation in coordination with a second PTM, O-GlcNAcylation. In this study, a further proteomic characterization of PPV CP phosphorylation revealed additional phospho-targets, thus evidencing even greater complexity of the network of PTMs affecting this protein. In particular, two new phosphorylation targets, T254 and T313, at protein distal core, appear to be highly relevant for infection. Although abolishing phosphorylation at these positions does not have a severe effect on infectivity or viral accumulation, phospho-mimicking at either of these targets disrupts cell-to-cell movement. Strand-specific reverse transcription-quantitative PCR analysis and fractionation by centrifugation in a continuous sucrose gradient enabled us to conclude that such a deleterious effect is not related to failures in replication but is a consequence of inaccurate virion assembly. The analysis of spontaneous compensatory mutations at the CP core identified in a multiple phospho-mimicking mutant disclosed a functional dialogue between distant phospho-targets, which was further supported by an in silico PPV virion model, built on the watermelon mosaic virus atomic structure. Therefore, whereas joint and opposite action of O-GlcNAcylation and phosphorylation at the N-terminal disordered protrusion of CP appears to regulate protein stability, we propose that phosphorylations at the core region control assembly and disassembly of viral particles.