The extraordinary diversification of beetles on Earth is a textbook example of adaptive evolution. Yet the tempo and drivers of this super-radiation remain largely unclear. Here, we address this problem by investigating the macroevolutionary dynamics in darkling beetles (Coleoptera: Tenebrionidae), one of the most ecomorphologically diverse beetle families (with >30k species). Using genomic datasets and multiple approaches, we resolve the long-standing inconsistency over deep relationships in the family. In conjunction with a landmark-based dataset of body shape morphology, we show that the evolutionary history of darkling beetles is marked by ancient rapid radiations, frequent ecological transitions, and rapid bursts of morphological diversification. On a global scale, our analyses uncovered a significant pulse of phenotypic diversification proximal to the K/Pg mass extinction and remarkable convergence of body shape associated with ecological specialization. On a regional scale, two major Australasian radiations, the Adeliini and the heleine clade, exhibited contrasting patterns of ecomorphological diversification, representing a clear contrast of phylogenetic niche conservatism versus adaptive radiation. Our findings align with the Simpsonian model of adaptive evolution across the macroevolutionary landscape and highlight a significant role of ecological opportunity in driving the immense ecomorphological diversity in a hyperdiverse beetle group.