Komagataella phaffii(Pichia pastoris) is a methylotrophic yeast that is favored by industry and academia mainly for expression of heterologous proteins. However, its full potential as a host for bio-production of valuable compounds is not yet fully exploited. The emergence of CRISPR-Cas9 technology has significantly improved the efficiency of gene manipulations of non-conventional species includingK. phaffii. Yet, improvements in gene-editing methods are desirable to further accelerate engineering of industrially and scientifically relevantK. phaffiistrains. In this study, we have developed a versatile one vector-based CRISPR-Cas9 method and showed that it works efficiently at different genetic loci using linear DNA fragments with very short targeting sequences. Importantly, we show that by using our setup it is possible to catalyze single-stranded oligonucleotide-mediated mutagenesis and marker-free gene integrations. Notably, we performed site-specific point mutations and full gene deletions using single stranded 90-mers at very high efficiencies. Lastly, we present a strategy for transient inactivation of non-homologous end-joining (NHEJ) pathway, whereKU70gene is disrupted by a visual marker (uidAgene). The latter system enables precise CRISPR-Cas9 based editing (including multiplexing) and accelerates selection of the mutants that have simultaneously undergone a desired genetic modification(s) and restored NHEJ-proficient genotype. In conclusion, the tools presented in this study can be applied for easy and efficient engineering ofK. phaffiistrains and could potentially be coupled with high-throughput automated workflows.