Various animals derive nutrients from symbiotic microorganisms with much-reduced genomes, but it is unknown whether, and how, the supply of these nutrients is regulated. Here, we demonstrate that the production of essential amino acids (EAAs) by the bacterium
Buchnera aphidicola
in the pea aphid
Acyrthosiphon pisum
is elevated when aphids are reared on diets from which that EAA are omitted, demonstrating that
Buchnera
scale EAA production to host demand. Quantitative proteomics of bacteriocytes (host cells bearing
Buchnera
) revealed that these metabolic changes are not accompanied by significant change in
Buchnera
or host proteins, suggesting that EAA production is regulated post-translationally. Bacteriocytes in aphids reared on diet lacking the EAA methionine had elevated concentrations of both methionine and the precursor cystathionine, indicating that methionine production is promoted by precursor supply and is not subject to feedback inhibition by methionine. Furthermore, methionine production by isolated
Buchnera
increased with increasing cystathionine concentration. We propose that
Buchnera
metabolism is poised for EAA production at certain maximal rates, and the realized release rate is determined by precursor supply from the host. The incidence of host regulation of symbiont nutritional function via supply of key nutritional inputs in other symbioses remains to be investigated.