Remodeling of host cellular membrane transport pathways is a common pathogenic trait of many intracellular microbes that is essential to their intravacuolar life cycle and proliferation. The bacterium Brucella abortus generates a host endoplasmic reticulum‐derived vacuole (rBCV) that supports its intracellular growth, via VirB Type IV secretion system‐mediated delivery of effector proteins, whose functions and mode of action are mostly unknown. Here, we show that the effector BspF specifically promotes Brucella replication within rBCVs by interfering with vesicular transport between the trans‐Golgi network (TGN) and recycling endocytic compartment. BspF targeted the recycling endosome, inhibited retrograde traffic to the TGN, and interacted with the Arf6 GTPase‐activating Protein (GAP) ACAP1 to dysregulate Arf6‐/Rab8a‐dependent transport within the recycling endosome, which resulted in accretion of TGN‐associated vesicles by rBCVs and enhanced bacterial growth. Altogether, these findings provide mechanistic insight into bacterial modulation of membrane transport used to promote their own proliferation within intracellular vacuoles. SYNOPSIS Host membrane transport remodeling via secreted effector proteins promotes proliferation of Brucella abortus bacteria within host cell vacuoles. Here, the effector BspF delivered by the Type IV secretion system is found to facilitate secretory vesicle rerouting by modulating Arf6/Rab8a GTPase signaling. BspF interferes with host cell retrograde membrane transport through the tubular recycling endosome. BspF binding to GTPase‐activating protein ACAP1 decreases Arf6/Rab8a‐dependent retrograde transport to the trans‐Golgi network (TGN). BspF modulation of retrograde transport facilitates Syntaxin‐6‐dependent recruitment of TGN‐associated vesicles to Brucella‐containing vacuoles, and facilitates bacterial growth. Brucella abortus effector protein BspF binding to host GTPase‐activating protein ACAP1 facilitates intracellular bacterial growth by decreasing retrograde vesicular transport to the trans‐Golgi network.