Understanding the effect of intricate surface wettability conditions on microswimmers is crucial for precisely navigating them across narrow microcirculatory networks. Here, we adopt the spherical squirmer model and Navier slip condition to delineate the microswimmer locomotion under a Poiseuille flow in a slit microchannel. Through a combined analytical–numerical approach utilizing bispherical coordinates and the superposition technique, we resolve the slip-modulated simultaneous hydrodynamic interaction with substrate boundaries. Phase portraits reveal that slip significantly alters propulsion mechanisms, destabilizing centreline stable oscillations of pullers beyond a threshold slip length. Superhydrophobic surfaces suppress near-wall rheotaxis states but preserve centreline focusing, facilitating slip-assisted directed transport without surface accumulation. Under strong background flows, subcritical Hopf bifurcation emerges for pullers at a critical slip length, transitioning dynamics from coexisting stable and unstable states to purely unstable behaviour. Contrastingly, for pushers, slip causes a transition from unstable to either stable or fixed-amplitude oscillations. Increased slip length reduces hydrodynamic repulsion on pullers from the walls by enhancing rotational velocity near the walls, whereas it counteracts the torque that causes unstable oscillations of pushers. Three-dimensional analysis of the trajectories reveals the significant role of the out-of-plane orientation of the microswimmer in its transitions between different swimming states. The presented regime maps offer parametric combinations for specific motion behaviours, guiding the development of smart microfluidic drug delivery systems and preventing biofilm deposition in biomedical devices.