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We report a microenvironment\u2010guided strategy for evolving phenotype\u2010specific molecular probes using single\u2010stranded DNA\u2010functionalized single\u2010walled carbon nanotubes (ssDNA\u2010SWCNTs). Our approach employs 3D tumor models that recapitulate complex cancer microenvironments, enabling identification of ssDNA sequences with differential binding properties. We developed two distinct probes for prostate cancer cells: PC3D2, which preferentially binds hypoxia\u2010adapted stem\u2010like cells associated with treatment resistance, and PC2D2, which shows enhanced binding to mesenchymal\u2010like cells. These probes exhibit characteristic second near\u2010infrared (NIR\u2010II, 1000\u20101700\u00a0nm) fluorescence, enabling non\u2010invasive detection of aggressive phenotypes in heterogeneous tumors using NIR\u2010II optical imaging. We demonstrate their utility for selective drug delivery to prostate cancer spheroids, resulting in enhanced therapeutic efficacy. 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