Toxoplasma gondii owes its unparalleled success as pathogen to a sophisticated arsenal of secretory organelles filled with virulence factors, concentrated at the parasite apex. The content of these micro-weapons, called micronemes and rhoptries, is used by the parasite to invade and take control of the host cell and subsequently, upon replicating, to escape from the host and find a new prey. Micronemes and rhoptries are secreted sequentially to fulfill distinct functions: microneme proteins ensure parasite egress, motility and host recognition, while rhoptry proteins are key for vacuole formation and subversion of host immune response. In addition, specific microneme and rhoptry proteins interact to form a tight junction at the host-parasite interface, supporting parasite entry into the host. Rhoptry discharge appears to rely on microneme secretion since the microneme protein MIC8 and the CLIP/CLAMP/SPATR microneme complex have been shown to have an exclusive role in regulating rhoptry release. We recently described Toxoplasma cysteine-repeat modular proteins CRMPa and CRMPb, which are part of a complex that comprises four essential mediators of rhoptry secretion. TgCRMPs and partners contain host cell binding domains and are translocated to the apical end of extracellular parasites at the onset of invasion, suggesting that they activate rhoptry discharge upon sensing the host. Here, we further characterize Toxoplasma CRMPs and investigate their possible association to micronemes. Using ultrastructure expansion microscopy (U-ExM), we confirm with a higher resolution that TgCRMPs show partial overlap with microneme markers. Their accumulation at the apical tip of extracellular parasites during invasion requires functional micronemes exocytosis, since it is abolished in parasites depleted of the TFP1 transporter that are defective in both biogenesis and secretion of micronemes. In addition, we show that TgCRMPs undergo proteolytic processing by the ASP3 protease, an enzyme responsible for the maturation of microneme and rhoptry factors. Altogether these data support a scenario where CRMPs traffic towards the parasite apex through micronemes and are then translocated in proximity of the rhoptry exocytic site upon microneme discharge.