Volatiles are of key importance for host-plant recognition in insects. In the pollination system of Lithophragma flowers and Greya moths, moths are highly specialized on Lithophragma, in which they oviposit and thereby pollinate the flowers. Floral volatiles in Lithophragma are highly variable between species and populations, and moths prefer to oviposit into Lithophragma flowers from populations of the local host species. Here we used gas chromatography coupled with electroantennographic detection (GC-EAD) to test whether Greya moths detect specific key volatiles or respond broadly to many volatiles of Lithophragma flowers. We also addressed whether olfactory detection in Greya moths varies across populations, consistent with a co-evolutionary scenario. We analyzed flower volatile samples from three different species and five populations of Lithophragma occurring across a 1400 km range in the Western USA, and their sympatric female Greya politella moths. We showed that Greya politella detect a broad range of Lithophragma volatiles, with a total of 23 compounds being EAD active. We chemically identified 15 of these, including the chiral 6, 10, 14-trimethylpentadecan-2-one (hexahydrofarnesyl acetone), which was not previously detected in Lithophragma. All investigated Lithophragma species produced the (6R, 10R)-enantiomer of this compound. We showed that Greya moths detected not only volatiles of their local Lithophragma plants, but also those from allopatric populations/species that they not encounter in local populations. In conclusion, the generalized detection of volatiles and a lack of co-divergence between volatiles and olfactory detection may be of selective advantage for moths in tracking hosts with rapidly evolving, chemically diverse floral volatiles.