In chloroplasts, binding of a c′-heme to cytochrome b$_6$ on the stromal side of the thylakoid membranes requires a specific mechanism distinct from the one at work for c-heme binding to cytochromes f and c$_6$ on the lumenal side of membranes. Here, we show that the major protein components of this pathway, the CCBs, are bona fide transmembrane proteins. We demonstrate their association in a series of hetero-oligomeric complexes, some of which interact transiently with cytochrome b$_6$ in the process of heme delivery to the apoprotein. In addition, we provide preliminary evidence for functional assembly of cytochrome b6f complexes even in the absence of c′-heme binding to cytochrome b$_6$. Finally, we present a sequential model for apo- to holo-cytochrome b$_6$ maturation integrated within the assembly pathway of b$_6$f complexes in the thylakoid membranes.