Astrophysical emission lines arising from particle decays can offer unique insights into the nature of dark matter (DM). Using dedicated simulations with background and foreground modeling, we comprehensively demonstrate that the recently launched X-Ray Imaging and Spectroscopy Mission (XRISM) space telescope with powerful X-ray spectroscopy capabilities is particularly well suited to probe decaying DM, such as sterile neutrinos and axion-like particles, in the mass range of a few to tens of keV. We analyze and map XRISM’s DM discovery potential parameter space by considering the Milky Way Galactic DM halo, including establishing an optimal line-of-sight search, as well as dwarf galaxies, where we identify Segue 1 as a remarkably promising target. We demonstrate that with only 100 ks exposure, the XRISM/Resolve instrument is capable of probing the underexplored DM parameter window around a few keV and testing DM couplings with a sensitivity that exceeds by two orders existing Segue 1 limits. Further, we demonstrate that XRISM/Xtend instrument sensitivity enables discovery of the nature of faint astrophysical X-ray sources, especially in Segue 1, which could shed light on star formation history. We discuss implications for decaying DM searches with improved detector energy resolution in future experiments.