Polymerization and organization of actin into complex superstructures is indispensable for structure and function of neuronal networks. This work shows that the F-actin-binding protein 1 (Abp1), which controls Arp2/3 complex-mediated actin nucleation via the neural Wiskott-Aldrich syndrome protein (N-WASP) and binds to postsynaptic scaffold proteins of the ProSAP/Shank family, has a profound impact on synaptic organization. RNAi mediated knock-down of Abp1 expression results in changes in early axon development virtually identical to Arp2/3 complex inhibition, i.e. a selective increase of axon length. This work reveals an essential role of Abp1 and its cooperation with Cdc42 in N-WASP-induced rearrangements of the neuronal cytoskeleton. Secondly, Abp1 controls the formation and morphology of dendritic spines harboring the postsynaptic signal reception and transduction apparatus. Overexpression of the two Abp1 F-actin-binding domains increases the length of spines but dramatically reduces mushroom-type spine density, due to lack of the Abp1 SH3 domain. In contrast, overexpression of full-length Abp1 increases mushroom spine and synapse density. This suggests that both actin-binding and SH3 domain interactions are crucial for Abp1’s role in spine maturation. Abp1 hereby works in close conjunction with ProSAP1/Shank2 and ProSAP2/Shank3, because ProSAP2 RNAi suppressed Abp1 effects, and the ProSAP/Shank-induced increase of spine head width is further promoted by Abp1 cooverexpression and reduced upon Abp1 knock-down. Spine head extension furthermore depends on local Arp2/3 complex-mediated actin polymerization, which is controlled by Abp1 via the Arp2/3 complex activator N-WASP. Abp1 thus plays an important role in the formation and morphology control of synapses by making a required functional connection between PSD components and postsynaptic actin dynamics. It furthermore is crucial for cytoskeletal processes underlying proper early neuronal network formation.