Cell state transitions play a pivotal role in the development of multicellular organisms, orchestrating the precise arrangement and abundance of distinct cell types within the organism. This critical task is carried out by gene regulatory networks, complex systems composed of molecular regulators including transcriptional activators, repressors, and their target genes. Unraveling the mechanisms by which these regulators drive such a precise and reliable process despite the random fluctuations intrinsic to any molecules is an intriguing question in developmental biology. In this thesis, I focus on the gene regulatory network of the highly-conserved Receptor Tyrosine Kinase (RTK)/ Mitogen-activated Protein Kinase (MAPK) pathway as a case study. Owing to decades of research, main components of the Drosophila RTK/MAPK signaling network are well-established. Here, I leverage the wealth of qualitative knowledge to gain quantitative insights on how the RTK/MAPK pathway effectors regulate cell state transitions in the developing Drosophila compound eye. The findings are consolidated into two results chapters. Chapter 2 focuses on elucidating how expression dynamics of the activator Pointed (Pnt) and repressor Yan - effectors of the Drosophila RTK/MAPK signaling pathway - are modulated to inform whether a progenitor cell remains in the multipotent state or differentiate into a photoreceptor neuron. Here I show that the expression ratio of Pnt to Yan in the nucleus is stabilized in the progenitor cell population, and that this activator-to-repressor ratio, not the absolute level of either transcription factor, determines the progenitor vs. photoreceptor neuron state. In Chapter 3, I delve deeper into how Pnt and Yan expression dynamics are used to fine-tune the transcriptional output at target loci. Specifically, I explore the regulation of two well-characterized photoreceptor-fate determining genes, spalt major and prospero at progenitor vs. photoreceptor fate decision windows. To this end, I developed a quantitative imaging and analysis pipeline that can simultaneously measure the abundance of proteins and nascent RNA at single nuclei resolution \textit{in vivo} developing Drosophila eye. Results suggest that the nuclear concentration of Yan may be used to determine whether the target gene promoter is in a transcriptionally active ("On") or inactive ("Off") state. Meanwhile, Pnt concentration is weakly correlated to the level of nascent transcripts produced from active promoters. In Chapter 4, I summarize the main findings presented in this thesis and discuss avenues for further exploration. Overall, my work explored how the interplay of antagonistic transcription factors Pnt and Yan contributes to the accuracy and robustness of cell fate decisions during complex tissue development. There are many examples in living cells where co-expressed transcription factors exert opposing regulatory inputs on a common set of target genes. The findings and the conceptual framework presented in this thesis may be relevant to other such systems. Finally,the experimental and computational analysis methods I developed may prove useful to the broader community using the developing Drosophila eye as a model system.