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ABSTRACT Chromosomal inversion polymorphisms are ubiquitous across the diversity of diploid organisms and play a significant role in the evolution of adaptations in those species. Inversions are thought to operate as supergenes by trapping adaptive alleles at multiple linked loci through the suppression of recombination. While there is now considerable support for the supergene mechanism of inversion evolution, the extent to which inversions trap pre‐existing adaptive genetic variation versus accumulate new adaptive variants over time remains unclear. In this study, we report new insights into the evolution of a locally adaptive chromosomal inversion polymorphism (inv_chr8A), which contributes to the adaptive divergence between coastal perennial and inland annual ecotypes of the yellow monkeyflower,Mimulus guttatus. This research was enabled by the sequencing, assembly and annotation of new annual and perennial genomes ofM. guttatususing Oxford Nanopore long‐read sequencing technology. In addition to the adaptive inv_chr8A inversion, we identified three other large inversion polymorphisms, including a previously unknown large inversion (inv_chr8B) nested within inv_chr8A. Through population genomic analyses, we determined that the nested inv_chr8B inversion is significantly older than the larger chromosomal inversion in which it resides. We also evaluated the potential role of key candidate genes underlying the phenotypic effects of inv_chr8A. These genes are involved in gibberellin biosynthesis and anthocyanin regulation. Although little evidence was found to suggest that inversion breakpoint mutations drive adaptive phenotypic effects, our findings do support the supergene mechanism of adaptation and suggest it may sometimes involve nested inversions that evolve at different times.