Recent high-resolution computational fluid dynamics (CFD) studies have detected persistent flow instability in intracranial aneurysms (IAs) that was not observed in previous in silico studies. These flow fluctuations have shown incidental association with rupture in a small aneurysm dataset. The aims of this study are to explore the capabilities and limitations of a commercial CFD solver in capturing such velocity fluctuations, whether fluctuation kinetic energy (fKE) as a marker to quantify such instability could be a potential parameter to predict aneurysm rupture, and what geometric parameters might be associated with such fluctuations. First, we confirmed that the second-order discretization schemes and high spatial and temporal resolutions are required to capture these aneurysmal flow fluctuations. Next, we analyzed 56 patient-specific middle cerebral artery (MCA) aneurysms (12 ruptured) by transient, high-resolution CFD simulations with a cycle-averaged, constant inflow boundary condition. Finally, to explore the mechanism by which such flow instabilities might arise, we investigated correlations between fKE and several aneurysm geometrical parameters. Our results show that flow instabilities were present in 8 of 56 MCA aneurysms, all of which were unruptured bifurcation aneurysms. Statistical analysis revealed that fKE could not differentiate ruptured from unruptured aneurysms. Thus, our study does not lend support to these flow instabilities (based on a cycle-averaged constant inflow as opposed to peak velocity) being a marker for rupture. We found a positive correlation between fKE and aneurysm size as well as size ratio. This suggests that the intrinsic flow instability may be associated with the breakdown of an inflow jet penetrating the aneurysm space.