In flies, the essential kinase JIL-1 responsible for most interphase H3S10ph is stabilized and targeted to chromatin by a new PWWP domain containing protein, which we called b-JIM. b-JIM binds JIL-1 within the conserved C-terminal domain which is still present Su(var)3-1 alleles of the JIL-1 gene and this binding is essential for the stability of JIL-1. The b-JIM/JIL-1 (JJ) complex is the major form of the kinase in vivo and interacts with other complexes implicated in the regulation of transcription. The most prominent new interactors, Dpy30L1 and BOD1 probably mediate the interaction with the Set1/COMPASS complex. We show that the JJ complex directly binds to H3K36me3 nucleosomes via the PWWP domain of b-JIM, and that this is the main mode of recruitment of JIL-1 to chromatin in vivo. Upon knock down of JIL-1 or the JJ complex, transcript levels from X-linked genes and many transposons are most prominently affected in male cells.