Abstract Species performance depends on the concerted interplay of their functional traits. Natural selection acts on the performance of the species and influences entire suits of interdependent functional traits, thereby driving the evolution of functional diversity (FD) within a clade. In a given habitat, interdependent functional traits are expected to integrate into only a few adaptive combinations. When a clade diversifies in different habitats, the FD within habitats (herein called α‐FD) diversifies in response to local selections, while between the habitats, alternative adaptive combinations of interdependent traits that are specific to the habitat emerge. This multivariate selection leads to two hypotheses. First, realized α‐FD within one habitat represents only a small fraction of the variation of functional traits, and second, realized FDs across habitats (hereafter called β‐FD) are equal to or greater than would be in the absence of the interdependence of functional traits. We tested these hypotheses using 185 species of the highly diverse subterranean amphipod genus Niphargus living in three habitats: river interstitial, cave lakes, and cave streams. We (i) explored integration of functional traits related to locomotion and feeding biology and tested (ii) if realized α‐FD within each habitat is lower than it would be without trait interdependence, and (iii) if realized β‐FD in pairwise comparisons of habitats is higher than it would be without trait interdependence. In all three habitats, the length of the appendages as a proxy of the locomotion speed was positively correlated with the trophic position of the species. On the contrary, the body shape correlations were habitat dependent: species in high trophic positions were slender, stout or invariant in shape in interstitial, cave streams and cave lakes, respectively. Using null models, we show that only a fraction of functional trait combinations was realized in each habitat, whereas β‐FD between habitats was equal to or greater than the null expectations. The results indicate preserved potential for diversification in species within and between habitats. This potential can be realized through hybridization and can drive diversification in adaptive radiations. Moreover, this perspective on the evolution of FD is compatible with several central ecological and evolutionary concepts, such as adaptive landscape or ecological niche theory. Read the free Plain Language Summary for this article on the Journal blog.