Socially exchanged fluids, such as seminal fluid and milk, are a direct means through which an organism can influence conspecifics. When orally feeding larval offspring via trophallaxis, workers of the carpenter ant Camponotus floridanus were recently shown to transfer Juvenile Hormone III (JH), a key developmental regulator, as well as paralogs of JH esterase (JHE), an enzyme that catalyzes degradation of JH. Here we combine proteomic, phylogenetic and selection analyses to investigate the evolution of this esterase subfamily. We show that members of the Camponotus JHE-like protein family have undergone multiple duplications, experienced positive selection, and changed tissue localization to become abundantly and selectively present in trophallactic fluid. The Camponotus trophallactic esterases have maintained their catalytic triads but contain a number of positively-selected amino acid changes distributed throughout the protein, which possibly reflect an adaptation to the highly acidic trophallactic fluid of formicine ants. To determine whether these esterases might regulate larval development, we fed workers with a JHE-specific pharmacological inhibitor to introduce it into the trophallactic network. This inhibitor increased the likelihood of pupation of the larvae reared by these workers, similar and complementary to supplementation with JH. Together, these findings suggest that JHE-like proteins have evolved new roles in the Camponotus genus in inter-individual regulation of larval development.