Actin depolymerizing factors (ADF/cofilin) modulate the rate of actin filament turnover, networking cellular signals into cytoskeletal-dependent developmental pathways. Plant and animal genomes encode families of diverse ancient ADF isovariants. One weakly but ubiquitously expressed member of the Arabidopsis ADF gene family, ADF9, is moderately expressed in the shoot apical meristem (SAM). Mutant alleles adf9-1 and adf9-2 showed a 95% and 50% reduction in transcript levels, respectively. Compared to wild-type, mutant seedlings and plants were significantly smaller and adult mutant plants had decreased numbers of lateral branches and a reduced ability to form callus. The mutants flowered very early during long-day light cycles, but not during short days. adf9-1showed a several-fold lower expression of FLOWERING LOCUS C (FLC), a master repressor of the transition to flowering, and increased expression of CONSTANS, an activator of flowering. Transgenic ADF9 expression complemented both developmental and gene expression phenotypes. FLC chromatin from adf9-1 plants contained reduced levels of histone H3 lysine 4 trimethylation and lysine 9 and 14 acetylation, as well as increased nucleosome occupancy consistent with a less active chromatin state. We propose that ADF9 networks both cytoplasmic and nuclear processes within the SAM to control multicellular development.