Understanding the evolutionary dynamics underlying herbivorous insect mega-diversity requires investigating the ability of insects to shift and adapt to different host plants. Feeding experiments with nine related stick insect species revealed that insects retain the ability to use ancestral host plants after shifting to novel hosts, with host plant shifts generating fundamental feeding niche expansions. These expansions were however not accompanied by expansions of the realized feeding niches, as species on novel hosts are generally ecologically specialized. For shifts from angiosperm to chemically challenging conifer hosts, generalist fundamental feeding niches even evolved jointly with strong host plant specialization, indicating that host plant specialization is not driven by constraints imposed by plant chemistry. By coupling analyses of plant chemical compounds, fundamental and ecological feeding niches in multiple insect species, we provide novel insights into the evolutionary dynamics of host range expansion and contraction in herbivorous insects.