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Transmitting tissue-specific proteins (TTS proteins) are abundant in the extracellular matrix of <i>Nicotiana</i> pistils, and vital for optimal pollen tube growth and seed set. We have identified orthologs from several species in the Solanaceae, including <i>Petunia</i> <i>axillaris axillaris</i> and <i>Petunia</i> <i>integrifolia</i>. We refer to TTS proteins and their orthologs as histidine domain-arabinogalactan proteins (HD-AGPs). HD-AGPs have distinctive domains, including a small histidine-rich region and a C-terminal PAC domain. Pairwise comparisons between HD-AGPs of 15 species belonging to <i>Petunia</i>, <i>Nicotiana</i>, and <i>Solanum</i> show that the his-domain and PAC domain are under purifying selection. In contrast, a proline-rich domain (HV2) is conserved among cross-hybridizing species, but variant in species-pairs that are reproductively isolated by post-pollination pre-fertilization reproductive barriers. In particular, variation in a tetrapeptide motif (XKPP) is systematically correlated with the presence of an interspecific reproductive barrier. Ka/Ks ratios are not informative at the infrageneric level, but the ratios reveal a clear signature of positive selection on two hypervariable domains (HV1 and HV2) when HD-AGPs from five solanaceous genera are compared. We propose that sequence divergence in the hypervariable domains of HD-AGPs reinforces sympatric speciation in incipient species that may have first diverged as a consequence of pollinator preferences or other ecological factors.