Significance Precise cell division is crucial for all cellular life. In the pneumococcus, which kills more than a million people annually, the protein MapZ was recently identified as a marker for the division site. By developing a suite of tools, including a chromosome labeling system and CRISPR/Cas9-based perturbation of chromosome segregation, we mapped the pneumococcal cell cycle in detail. We show that MapZ is not involved in division site selection but is important for setting the correct angle of the division plane. Importantly, we demonstrate that the pneumococcus has a unique chromosomal organization and that timely replication and segregation of the chromosomal origin to the future cell division site is a key determinant for correct positioning of cell division proteins.