Plants sense and respond to microbes utilizing a multilayered signalling cascade. In seed plants, the phytohormones jasmonic and salicylic acid (JA and SA) are key denominators of how plants respond to certain microbes. Their interplay is especially well-known for tipping the scales in plants' strategies of dealing with phytopathogens. In non-angiosperm lineages, the interplay is less well understood, but current data indicate that it is intertwined to a lesser extent and the canonical JA/SA antagonism appears to be absent. Here, we used the water fern Azolla filiculoides to gain insights into the fern's JA/SA signalling and the molecular communication with its unique nitrogen fixing cyanobiont Nostoc azollae, which the fern inherits both during sexual and vegetative reproduction. By mining large-scale sequencing data, we demonstrate that Azolla has most of the genetic repertoire to produce and sense JA and SA. Using qRT-PCR on the identified biosynthesis and signalling marker genes, we show that Azolla is responsive to exogenously applied SA. Furthermore, exogenous SA application influenced the abundance and gene expression of Azolla's cyanobiont. Our data provide a framework for JA/SA signalling in ferns and suggest that SA might be involved in Azolla's communication with its vertically inherited cyanobiont.