Spermatozoa may provide insights into the evolutionary history, reproductive isolation, and mating systems of species. Here we combine sperm and genomic data to conduct the first comparative analysis of sperm differentiation among Darwin’s finches, an iconic adaptive radiation with considerable gene flow across species borders. All eight study species had the typical form of songbird spermatozoa, but shorter than most other species in the Thraupidae family. There was no detectable differentiation in sperm length among four ground finch species (Geospiza) and two tree finch species (Camarhynchus). In both genera, autosomal single nucleotide polymorphisms (SNPs) revealed signatures of genetic admixture. The grey warbler-finch Certhidea fusca and the vegetarian finch Platyspiza crassirostris had significantly shorter sperm than the sister genera Geospiza and Camarhynchus from which they diverged about 0.90 and 0.43 Mya, respectively. The largest intergeneric divergences in sperm length were of the same magnitude as divergences observed within the speciation continuum in other songbirds over similar time spans. Relatively high among-male variation in sperm length indicates a moderate-to-low level of extrapair paternity and a divergence rate in sperm length that is lower than in more promiscuous songbirds. We conclude that sperm size evolution is too slow to drive prezygotic isolation in this radiation.