Date palm (Phoenixdactylifera) is the most significant crop across North Africa and the Middle East. However, the crop faces a severe threat from Bayoud disease caused by the fungal pathogen Fusarium oxysporum f. sp. albedinis (FOA). FOA is a soil-borne fungus that infects the roots and vascular system of date palms, leading to widespread destruction of date palm plantations in North Africa over the last century. This is considered the most devastating pathogen of oasis agriculture in North Africa and responsible for loss of 13 million trees in Algeria and Morocco alone. In this study, we present a chromosome-scale high-quality genome assembly of the virulent isolate Foa 44, which provides valuable insights into understanding the genetic basis of Bayoud disease. The genome assembly consists of 11 chromosomes and 40 unplaced contigs, totalling 65,971,825 base pairs in size. It exhibits a GC ratio of 47.77% and a TE (transposable element) content of 17.30%. Through prediction and annotation, we identified 20,416 protein-coding genes. By combining gene and repeat densities analysis with alignment to Fusarium oxysporum f. sp. lycopersici (FOL) 4287 isolate genome sequence, we determined the core and lineage-specific compartments in Foa 44, shedding light on the genome structure of this pathogen. Furthermore, a phylogenomic analysis based on the 3,292 BUSCOs core genome revealed a distinct clade of FOA isolates within the Fusarium oxysporum species complex (FOSC). Notably, the genealogies of the five identified Secreted In Xylem (SIX) genes (1, 6, 9, 11 and 14) in FOA displayed a polyphyletic pattern, suggesting a horizontal inheritance of these effectors. These findings provide a valuable genomics toolbox for further research aimed at combatting the serious biotic constraints posed by FOA to date palm. This will pave the way for a deeper understanding of Bayoud disease and facilitate the development of effective diagnostic tools and control measures.