Motility of unicellular algal cells, especially its ability to respond to environmental cues, is crucial in industrial and ecological contexts and has been studied extensively with the model organism Chlamydomonas. However, little is known about the relationship between motility and the cell-cycle, despite the apparent link of mitosis dependent morphological changes which involve the flagella and the dependency on light/dark conditions of the cellular reactions. In this study, the cell swimming speed, the rotational diffusivity and its swimming bias against gravity were measured with high-speed video microscopy with Chlamydomonas reinhardtii cultures highly synchronised to a diurnal cycle. A simulation of gravitactic cell trajectories was developed to assist the statistical analysis of the cell trajectories from the images, which subject to a projection effect and has not been addressed previously. Its morphological changes, including cell size, shape, mass density, and presence of flagella were also evaluated. Un unforeseen change of cell motility at a critical mitosis time point was discovered, and our analysis suggests a connection to the alternating cell energetic regimes rather than the cell morphology. As indicated by results obtained from imaging based experimental measurements and by computational methods, the motility variation has direct consequences on the collective motion of algal cells in a Hagen–Poiseuille flow, a relevant component flow for air-lift photobioreactors. The cell number density profiles were calculated by an individual-based simulation and a continuum system inclusive of the buoyancy effect imposed by the aggregated cells on their surrounding fluid. Qualitative experimental-theoretical agreement suggests that the models can be employed for optimisation problems of photobioreactor flow designs inclusive of the non-negligible cell-cycle effects, which has been commonly overlooked in previous studies.