Asexual reproduction is expected to reduce the adaptive potential to novel or changing environmental conditions, restricting or altering the ecological niche of asexual lineages. Asexual lineages of plants and animals are typically polyploid, an attribute that may influence their genetic variation, plasticity, adaptive potential, and niche breadth. The genus Boechera (Brassicaceae) represents an ideal model to test the relative ecological and biogeographic impacts of reproductive mode and ploidy because it is composed of diploid sexual and both diploid and polyploid asexual (i.e., apomictic) lineages. Here, we demonstrate a strong association between a transcriptionally conserved allele and apomictic seed formation. We then use this allele as a proxy apomixis marker in 1,649 accessions to demonstrate that apomixis is likely to be a common feature across the Boechera phylogeny. Phylogeographic analyses of these data demonstrate (i) species-specific niche differentiation in sexuals, (ii) extensive niche conservation between differing reproductive modes of the same species, (iii) ploidy-specific niche differentiation within and among species, and (iv) occasional niche drift between apomicts and their sexual ancestors. We conclude that ploidy is a substantially stronger and more common driver of niche divergence within and across Boechera species although variation in both traits may not necessarily lead to niche evolution on the species scale.