Invasive listeriosis is relatively rare, but is one of the deadliest food-borne infections, affecting pregnant women, their fetuses and newborn infants, the elderly and immunocompromised people. The aim of this study was to research the impact of the COVID-19 pandemic on invasive listeriosis in the metropolis. Loci and whole-genome sequencing with subsequent bioinformatic analysis were used for the study of clinical and food Listeria monocytogenes isolates revealed in 2018–2022. The results indicate the crucial change in the spectrum of the L. monocytogenes sequence types (ST) causing invasive listeriosis during the COVID-19 pandemic, with slight changes in the ST spectrum of the food isolates. An increase in sensitivity to previously non-human L. monocytogenes genotypes, namely ST8, 20, 21, 37, 391, and 425, was observed. L. monocytogenes of ST20 and 425 carried plasmids with virulence factors (VF), in addition to the 42 VF identified in the genomes with the vip gene exclusion in the genomes of ST7, 8, 21, and 37. Perinatal listeriosis cases were associated with the new hypervirulent L. monocytogenes of ST1, 4, and 219 compiled with old ST6. These data indicate the need for the more stringent control of food products for high-risk groups.