The development of in transit metastases of melanoma (ITM) presents a unique clinical challenge given the potential of these metastatic lesions to disseminate and their propensity to recur. While immune checkpoint blockade (ICB) therapies have improved outcomes, half of patients treated will have resistant disease and little is known about the mechanisms, particularly within the setting of ITM disease. ITM disease offers a unique clinical and cellular landscape to study the underlying biology of ITM and the influence of ICB on disease progression. Here, we apply single cell multiomics on ITM biopsies from patients that received anti-PD-1 monotherapy or combination anti-PD-1+CTLA-4 therapies. We find a cellular landscape dominated by melanocytes with limited immune and stromal cell infiltration. We observed that genetic diversity and dedifferentiation within the melanocyte compartment associated with ICB resistance and disease progression. Conversely, T cell clonal expansion and clone sharing among specific tissue-resident memory T cell subsets were associated with ICB response. Our results provide the first multiomic cellular examination of ITM in the context of ICB and reinforce the importance of genomic and cellular heterogeneity in ICB response, resistance, and disease progression. These insights may inform the development of novel therapeutic strategies to overcome ICB resistance and improve outcomes for patients with ITM disease.