The proposed DarkQuest beam dump experiment, a modest upgrade to the existing SeaQuest/SpinQuest experiment, has great potential for uncovering new physics within a dark sector. We explore both the near-term and long-term prospects for observing two distinct, highly-motivated hidden sector benchmark models: heavy neutral leptons and Higgs-mixed scalars. We comprehensively examine the particle production and detector acceptance at DarkQuest, including an updated treatment of meson production, and light scalar production through both bremsstrahlung and gluon-gluon fusion. In both benchmark models, DarkQuest will provide an opportunity to probe previously inaccessible interesting regions of parameter space on a fairly short timescale when compared to other proposed experiments.