Apple proliferation disease is caused by the phloem-dwelling bacterium ‘Candidatus Phytoplasma mali’, inducing morphological changes in its host plant apple, such as witches’ broom formation. Furthermore, it triggers physiological alterations like emission of volatile organic compounds or phytohormone levels in the plant. In our study, we assessed phytoplasma-induced changes in the phloem by sampling phloem sap from infected and non-infected apple plants. In infected plants, the soluble sugar content increased and the composition of phloem metabolites differed significantly between non-infected and infected plants. Sugar and sugar alcohol levels increased in diseased plants, while organic and amino acid content remained constant. As ‘Ca. P. mali’ is vectored by the phloem-feeding insect Cacopsylla picta (Foerster, 1848), we assessed whether the insect–plant interaction was affected by ‘Ca. P. mali’ infection of the common host plant Malus domestica Borkh. Binary-choice oviposition bioassays between infected and non-infected apple leaves revealed C. picta’s preference for non-infected leaves. It is assumed and discussed that the changes in vector behavior are attributable to plant-mediated effects of the phytoplasma infection.