Abstract While most galaxies appear to host a central supermassive black hole (SMBH), they are expected to also contain a substantial population of off-center “wandering” SMBHs naturally produced by the hierarchical merger-driven process of galaxy assembly. This population has been recently characterized in an analysis of the Romulus cosmological simulations, which correct for the dynamical forces on SMBHs without artificially pinning them to halo centers. Here we predict an array of electromagnetic signatures for these wanderers. The predicted wandering population of SMBHs from Romulus broadly reproduces the observed spatial offsets of a recent sample of hyperluminous X-ray sources. We predict that the sources with the most extreme offsets are likely to arise from SMBHs within satellite galaxies. These simulations also predict a significant population of secondary active galactic nuclei (AGNs) with luminosities at least 10% that of the central AGN. The majority of galaxies at z = 4 that host a central AGN with bolometric luminosity L bol > 1042 erg s−1 are predicted to host a companion off-center AGN of comparable brightness. We demonstrate that stacked X-ray observations of similar mass galaxies may reveal a halo of collective emission attributable to these wanderers. Finally, because wanderers dominate the population of SMBHs with masses of ≲107 M ⊙ in Romulus, they may dominate tidal disruption event (TDE) rates at these masses if they retain a stellar component (e.g., a nuclear star cluster). This could warrant an order of magnitude correction to current theoretically estimated TDE rates at low SMBH masses.