We explored the inter- and intrapopulation variability in the larval defensive chemistry of the leaf beetle Chrysomela lapponica with respect to the salicylic glycoside (SG) content of its host species. Secretions of larvae from three populations associated in nature with SG-poor willows contained nearly twice as many components and 40-fold higher concentrations of autogenously produced isobutyrates and 2-methylbutyrates than secretions of larvae from three populations associated with SG-rich willows, which in turn had 200-fold higher concentrations of host-derived salicylaldehyde. Reciprocal transfer experiments showed that the larvae from populations associated with SG-rich willows did not produce appreciable amounts of butyrates on either SG-rich or SG-poor willows, while populations feeding on several SG-poor willow species retained the ability for efficient sequestration of SGs, along with their ability to produce high amounts of isobutyrates and 2-methylbutyrates. Only the populations associated with SG-poor willows demonstrated among-family variation in the composition of defensive secretion and differential responses of individual families to willows with alternative SG levels, which can be seen as the prerequisites for shifting to novel hosts. These non-specialized populations show a dual defensive strategy, which corresponds to the ancestral state of this species, while populations that fully depend on host-derived toxins (feeding on SG-rich willows) or have lost the ability to produce salicylaldehyde (feeding on birches) are most deviant from the ancestral state. The results indicate that defensive strategies may differ between populations within a species, and suggest that this variation reduces extinction risks and maintains the high ecological diversity and wide distribution of C. lapponica.