The Cajal body (CB) is an evolutionarily conserved nuclear subcompartment, enriched in components of the RNA processing machinery. The composition and dynamics of CBs in cells of living organisms is not well understood. Here we establish the zebrafish embryo as a model system to investigate the properties of CBs during rapid growth and cell division, taking advantage of the ease of live-cell imaging. We show that zebrafish embryo CBs contain coilin and multiple components of the pre-mRNA splicing machinery. Histone mRNA 3' end processing factors, present in CBs in some systems, were instead concentrated in a distinct nuclear body. CBs were present in embryos before and after activation of zygotic gene expression, indicating a maternal contribution of CB components. During the first 24 hours of development, embryonic cells displayed up to 30 CBs per nucleus; these dispersed prior to mitosis and reassembled within minutes upon daughter cell nucleus formation. Following zygotic genome activation, snRNP biogenesis was required for CB assembly and maintenance, suggesting a self-assembly process that determines CB numbers in embryos. Differentiation into muscle, neurons and epidermis was associated with the achievement of a steady state number of 2 CBs per nucleus. We propose that CB number is regulated during development to respond to the demands of gene expression in a rapidly growing embryo.