In fast-evolving neural circuits like the olfactory system, some neuronal lineages, and their developmental programs may be more variable, for better adaptability to the environment, while others may be more stable to conserve important functions. To test this, we conducted a comparative analysis of the olfactory system transcriptome of four different Drosophila species at multiple points during development. Our analysis revealed that the olfactory receptor neurons (ORNs) expressing Or22a show the highest variation in developmental and transcriptional programs. Interestingly, Or22a ORNs play an important role in the chemosensory adaptations of specialist feeder species to their host plants. Or22a receptor detects host plant odors, and the number of Or22a neurons and their target antennal lobe glomeruli in the brain are increased in both species. To determine whether the species-specific variation in Or22a ORN lineage, number and gene expression is also represented in their developmental program, we analyzed three classes of transcription factors acting at three stages of ORN development: 1) prepatterning transcription factors, which we recently found to partition the antennal disc into multiple rings each with a restricted developmental potential; 2) proneural genes, whose expression selects specific cells from these rings to become the precursors to form specific sensilla and the ORNs they house; and 3) terminal selector transcription factors that regulate olfactory receptor gene expression. Among these three regulatory classes of transcription factors in ORN fate determination, we found the pre-patterning transcription factors to be the most dynamic, both individually and in combinations, across species during development, especially for the combinations that generate the ab3 fate. In contrast, other ORN lineages are very stable both in number and gene expression profiles regulating their identity and developmental programs. Interestingly, pairwise comparison of the developmental gene expression profiles of olfactory system in four species showed that the specialists species are also the more similar in each other then they are to the generalist species. Together, these studies suggest that not only is variation in structural properties of Or22a ORNs associated with behavioral variation, but that this variation is also reflected in the developmental programs culminating in Or22a ORNs fates. Together, these findings may shed light on variation and plasticity in development of specific ORN lineages that may facilitate the adaptation of Drosophila chemosensory behaviors to specific ecological niches.