The vertebrate sense of smell employs four major and several minor olfactory receptor families, with staggered evolutionary origins in cephalochordates (ORs), the common ancestor of vertebrates (TAARs and V1Rs, adorb/A2C) or the common ancestor of jawed fish (TAARs and V2Rs). We have taken advantage of the recent availability of high quality genomic databases of early-derived chordates to re-assess the origin of these olfactory receptor families. We clarify the TAAR receptors of lamprey (jawless vertebrate) as a TAAR-like sister clade to the TAAR family of jawed vertebrates (TARL). This sister clade is also present in jawed vertebrates but there it has not undergone gene expansion and is not expressed in olfactory sensory neurons. We show the lamprey V1R family to consist of six genes, one of them a direct ortholog of a gene conserved in bony fish. We report the presence of one to two V2R receptors in lampreys, thus backdating the origin of the V2R family to the common ancestor of vertebrates. Moreover we show that adorb is present already in cephalochordates (lancelets), hemichordates (acorn worms) and echinoderms (sea stars and sea urchins), suggesting its presence in the common ancestor of deuterostomes. Neither lamprey V2Rs nor lamprey adorb are expressed in olfactory sensory neurons. We conclude that the evolutionary origin of V2Rs, TARL, and adorb/A2C olfactory receptors is dissociated from the origin of their function as olfactory receptor.