1. Novel hosts present phytophagous insects with nutritional challenges which can cause host‐associated divergence. 2. The performance of the Bog gum‐Victorian metapopulation of Ctenarytaina bipartita Burckhardt et al. (Psylloidea:Aphalaridae), a psyllid whose range is being expanded by tree planting, on five species and genotypes of Eucalyptus endemic to south‐eastern Australia was quantified. Settling of females on two non‐hosts was also tested. 3. Female C. bipartita exhibited significant host‐associated plasticity in proctiger length (the body part used for oviposition into apical buds). Psyllids with longer wings and proctigers arose from a primary host. Fecundity varied significantly among hosts and was highest on a novel host. Hosts did not differ significantly in free amino acids (FAAs) but did differ in concentrations of essential amino acids (EAAs). However, nymphs did not differ significantly in EAAs. Surprisingly, fecundity was not related to total FAAs, availability of EAAs or concentrations of EAAs but was related to concentrations of four non‐EAAs. Mean fecundity per host was also positively related to the relative abundance of galloyl groups (associated with hydrolysable tannins). 4. Leaf age was more important to settling than eucalypt species; females settled on young leaves but this response was not related to leaf water content. 5. Planting the rare Eucalyptus kitsoniana in new habitats will expand the range of Bog gum‐Victorian C. bipartita and provide a bridge for the colonisation of novel eucalypts with buds suitable for oviposition. Host expansion by this metapopulation is not constrained by nutritional quality and may result in morphological divergence.