Primary cilia mediate signal transduction by acting as an organizing scaffold for cell membrane receptors, signaling proteins, and ion channels. Ciliated olfactory sensory neurons (OSNs) organize olfactory G-protein coupled receptors and ion channels on dendritic cilia and generate a cAMP-coupled influx of calcium ions as a primary signal in odorant detection. In the zebrafish olfactory placode, ciliated OSNs and microvillus OSNs constitute the major OSN cell types with reported distinct odorant sensitivity. Here we report single cell analysis of transgenic zebrafish expressing the calcium indicator GCaMP5 in OSNs to directly image cilia-dependent OSN responses to odorants in live zebrafish larvae. Oval/ift88 mutant (ift88 -/-) and ift172 knock-down zebrafish showed fewer and severely shortened OSN cilia without a reduction in total OSN number. OSN response amplitude to bile acids, and food odor were significantly reduced in ift88 mutants and ift172-deficient embryos while the responses to amino acids were not significantly changed. We have also generated CRISPR/Cas9 mutants of the syndromic ciliopathy genes Cep290 and BBS4 which show delayed defects specifically in sensory cilia structures. Combining ciliopathy gene mutations with biosensor transgenes provides a quantitative model for studying sensory ciliogenesis in zebrafish and a platform for therapeutic screening. Our results also implicate ift172-deficiency as a novel cause of anosmia.