From November 1919 Jakac studied painting and graphic arts at the Academy of Fine Arts in Prague (under professors Jakub Obrovský and Franz Thiele). There, he came into contact with rich artistic tradition and versatile modern art movements that expanded his artistic horizons tremendously. During that period he also visited Paris and Bremen. He finished the postgraduate studies of graphic arts under professor August Brömse.
In 1920 Jakac returned to Novo Mesto and became the bearer of The Spring of Novo Mesto, an avant-garde movement in literature and fine arts, which included also the poets Miran Jarc and Anton Podbevšek, painter Ivan Čargo and composer Marij Kogoj. In 1924 he settled in Ljubljana. At first, he earned his money as a woodcut illustrator at the liberal newspaper Jutro and a professor of drawing at the Second State Gymnasium in Ljubljana. Three years later he gave up his work and became an independent artist. At that time he also travelled extensively, for example to Paris, Tunisia, the Americas and Norway, and married Tatjana Gudrunova who influenced his work profoundly. In 1932, he published his memoirs and letters from America in a book entitled Odmevi rdeče zemlje ("Echoes of the Red Earth") in cooperation with his friend Miran Jarc.
In September 1943 Jakac joined the partisan resistance in the Province of Ljubljana, where he promoted culture and education and noted the events in numerous graphics. In 1943 he participated as a deputy in the Assembly of Delegates of the Slovenian Nation in Kočevje, which was a general constitutional convention organized by the Liberation Front of the Slovenian People in order to establish the legal basis for future political sovereignty. That year he was also among the Slovene deputies at the second AVNOJ Conference in Jajce. At that time he contributed significantly to the establishment of Ljubljana Academy of Fine Arts, which was realised in 1945, and then served as its dean for three mandates (1945-1947, 1947-1949 and later in 1959-1961) and taught graphic arts till his retirement in 1961.
In 1949 Jakac became a full member of Slovene Academy of Sciences and Arts. In addition, in 1963 he became a correspondent member of the Yugoslav Academy of Sciences and Arts in Zagreb and a correspondent member of the Serbian Academy of Sciences and Arts in Belgrade (1963). He was also the president of the Association of Fine Artists of Yugoslavia, a republican and federal deputy, and the initiator of the International Biennal of Graphic Art in Ljubljana.
Jakac died in Ljubljana in 1989 and is buried in Novo Mesto.
In his teenager years, he created watercolors of scenes from nature and of the Novo Mesto landscape, distinguished by reduced Realism, Mood Impressionism and the exploration of light effects, as well as by discovery and establishment of his pastel technique.
After the depature to Prague he progressed rapidly in his artistic development and incorporated many of the elements of Cubism, Expressionism and Abstract art in his works. Although he liked to picture the landscape of the Czech lands, he preferred the poetic landscape of his home region Lower Carniola (Dolenjska), full of shades and veiled atmosphere.
On his travels abroad in the 1930s, Jakac photographed and painted what he saw, giving his work an important documentary value. His art slowly transformed itself into lyrical realism.
Jakac was an excellent portraitist who depicted a number of prominent Slovenes and Yugoslavs, friends and very often also himself. In 1940 he painted a portrait of the Slovenian poet France Prešeren, which became one of the emblematic rafigurations of the national poet. In the 1970s, his portraits were used in a series of Yugoslav postage stamps.
After the war Jakac continued to paint landscapes of the dynamic Lower Carniola. Some of Jakac's best works (The Teran Vine, The Last Stars) originate from his late period, when he created symbolistically-charged colored woodcuts.
Jakac was essentially a black-and-white artist. His favourite painting technique was chalk pastel, which appealed to him due to its mellowness and the possibility for quick painting during his numerous travels.
Today, many of the works of Jakac are permanently exhibited in Božidar Jakac Gallery in Kostanjevica na Krki and in Jakac House in Novo Mesto. His films are kept by the Archives of the Republic of Slovenia.
Jakac was named the honorary academician of Accademia dell'Arte del Disegno in Florence (1965) and a full member of European Academy of Arts, Sciences and Humanities in Paris (1982). In 1959, he was the first person bestowed the title of the honorary freeman of Novo Mesto.