Cultural evolution may accelerate speciation, but most support for this hypothesis is limited to cases of allopatric speciation through random cultural drift. In contrast, cultural evolution’s role in non-allopatric speciation (i.e., speciation with gene flow) has been less explored. One clade in which cultural evolution may have figured prominently in speciation with gene flow includes the conifer-seed-eating finches in the red crossbill (Loxia curvirostra) complex. Here we focus on Cassia crossbills (L. sinesciuris; an ecotype recently split taxonomically from red crossbills) that learn social contact calls from their parents. Previous work found that individuals modify their calls throughout life such that they become increasingly divergent from a sympatric red crossbill ecotype. This open-ended modification of calls could lead to character displacement if it causes population-level divergence in call structure that, in turn, reduces maladaptive heterospecific flocking. Heterospecific flocking is maladaptive because crossbills use public information from flockmates to assess resource quality, and feeding rates are depressed when flockmates differ in their ability to exploit a shared resource (i.e., when flockmates are heterospecifics). We confirm the predictions of character displacement by documenting substantial population-level divergence in Cassia crossbill call structure over two decades, and by using field experiments that demonstrate a reduction in heterospecific flock formation in response to recent call divergence. Because crossbills choose mates from within flocks, a reduction in heterospecific flocking should increase assortative mating and may have been critical for speciation of Cassia crossbills in the face of ongoing gene flow in as few as 5,000 years. Our results provide evidence for a novel and potentially widespread mechanism by which reproductive isolation can evolve between sympatric lineages as a byproduct of adaptive cultural evolution.