Long-term field surveys on the distribution and natural infection rates of Cacopsylla melanoneura were carried out in commercial and abandoned apple-proliferation-infected orchards throughout Germany, northern Switzerland, and eastern France. Although the infection rates of some orchards reached up to 80%, only 0.09% of all C. melanoneura collected on apple were infected by the pathogen ‘Candidatus Phytoplasma mali’. Despite higher population densities, no infected individual was found on wild hawthorn. Individuals of C. melanoneura were not able to transmit phytoplasmas to healthy plants, and even the acquisition of ‘Ca. P. mali’ from infected plants was very inefficient. Quantitative real-time polymerase chain reaction demonstrated that the very few infected individuals of C. melanoneura harbored phytoplasma concentrations 10,000 times lower than individuals of C. picta, the main vector species in Germany. Oviposition bioassays showed that hawthorn is the preferred reproduction host plant for C. melanoneura in Germany, not apple. Because hawthorn is not a suitable host plant for ‘Ca. P. mali’, it does not play a role in the spread of apple proliferation. In contrast to data reported from northwestern Italy, C. melanoneura developed on either apple or hawthorn has no relevance as a vector of apple proliferation in Germany. The existence of epidemiologically different populations is proposed.