Current theories on the role of serotonin (5‐HT) in vertebrate defensive behavior suggest that this monoamine increases anxiety but decreases fear, by acting at different levels of the neuroaxis. This paradoxical, dual role of 5‐HT suggests that a serotonergic tone inhibits fear responses, while an acute increase in 5‐HT would produce anxiety‐like behavior. However, so far no evidence for a serotonergic tone has been found. Using zebrafish alarm responses, we investigate the participation of phasic and tonic 5‐HT levels in fear‐like behavior, as well as in behavior after stimulation. Conspecific alarm substance (CAS) increased bottom‐dwelling and erratic swimming, and animals transferred to a novel environment after CAS exposure (post‐exposure behavior) showed increased bottom‐dwelling and freezing. Clonazepam blocked CAS effects during and after exposure. Acute fluoxetine dose‐dependently decreased fear‐like behavior, but increased post‐exposure freezing. Metergoline had no effect on fear‐like behavior, but blocked the effects of CAS on post‐exposure behavior; similar effects were observed with para‐chlorophenylalanine. Finally, CAS was shown to decrease the activity of monoamine oxidase in the zebrafish brain after exposure. These results suggest that phasic and tonic serotonin encode an aversive expectation value, switching behavior toward cautious exploration/risk assessment/anxiety when the aversive stimulus is no longer present. Hypothetical mechanism of the serotonergic signaling in zebrafish defensive behavior during and after exposure to conspecific alarm substance (CAS). CAS elicits responses dominated by erratic swimming, which decreases as the substance's concentrations decline. After CAS exposure, the behavioral response is dominated by freezing. Serotonin (5‐HT) shifts responding from the first to the second (represented by the purple arrow, as well as by the arrows connecting the raphe to the “switch” green boxes), putatively by switching control from the mesencephalic aversive circuit (“switch OFF”) to the prosencephalic aversive circuit (“switch ON”).