The diamondback moth, Plutella xylostella, has been intensively studied due to its ability to evolve insecticide resistance and status as the world’s most destructive pest of brassicaceous crops. The surprise discovery of a cryptic ally, Plutella australiana Landry & Hebert, with apparent endemism to Australia, immediately raised questions regarding the extent of ecological and genetic diversity between these two species, whether gene flow could occur, and ultimately if specific management was required. Here, we show that despite sympatric distributions and the capacity to hybridize in controlled laboratory experiments, striking differences in genetic and phenotypic traits exist that are consistent with contrasting colonization histories and reproductive isolation after secondary contact. Almost 1500 Plutella individuals were collected from wild and cultivated brassicaceous plants at 75 locations throughout Australia. Plutella australiana was commonly found on all Brassica host types sampled except commercial vegetables, which are routinely sprayed with insecticide. Bioassays using four commonly-used insecticides found that P. australiana was 19-306 fold more susceptible than P. xylostella. Genome-wide SNPs derived from RADseq revealed substantially higher levels of genetic diversity across P. australiana compared with P. xylostella nuclear genomes, yet both species showed limited variation in mtDNA. Infection with a single Wolbachia subgroup B strain was fixed in P. australiana, suggesting that a selective sweep contributed to low mtDNA diversity, while a subgroup A strain infected just 1.5 % of P. xylostella. Although P. australiana is a potential pest of brassica crops, it is of secondary importance to P. xylostella.