First held August 10 to 15, 1976, the OIAF created a gathering place for North American animation professionals and enthusiasts to ponder the craft and business of animation. It also provided their international colleagues with a unique opportunity to gain an appreciation for and access to the North American scene.

Many key players of Canadian animation banded together to help festival founders, Bill Kuhns (who came up with the idea for a festival), Frederik Manter, Prescott J. Wright, Frank Taylor and the late Kelly O'Brien (who put it all together) organize North America's first event of its kind. The National Film Board of Canada, Radio Canada, CBC Television, and Cinémathèque Québécoise, among others, all had a hand in creating and building what is now North America's largest animation festival.

Canada's capital was a natural choice for an international animation festival. Home to animation innovator Norman McLaren, some of Canada's first private animation studios, and the former headquarters of the National Film Board, Ottawa's animation community provided a nurturing atmosphere for the fledgling festival.

Main events of the first festival included screenings of films entered in and out of competition; a Forum for the Future seminar; a NFB art exhibition; Oskar Fischinger; Raoul Barré, and Fleischer Brothers retrospectives; cut-collage and children's film compilations; hands-on animation workshops for young animators lead by Co Hoedeman, Peter Foldes, and Caroline Leaf (imagine!); plus the world premiere of Italian animator Bruno Bozzetto's first feature film Allegro Non Troppo .

Norman McLaren served as the festival's first honorary president, a tribute that has been bestowed to legendary animators like Frédéric Back (1984), David Ehrlich (2002), and Co Hoedeman (2004), among others.

The Animators Picnic, first held in 1976, became the social highlight of every festival, with animators – Oscar winners among them – fiercely competing for the best-carved pumpkin prize. Chez Ani, the nightly animators café founded by Co Hoedeman, at the second festival in 1978, continues to provide festival participants with a place to unwind, meet with friends old and new, and broker the occasional deal.

Since the beginning, the OIAF has put out a call for entries for films to compete for festival prizes, including the prestigious Grand Prize, the festival's highest honour. Given the growing number of entries received over the years, the popularity and need for the festival has never been in doubt. Beginning with just over 400 films at the 1976 festival, the number of entries received for OIAF 07 was a record-breaking 2,078 films, the most entries ever received by any international animation festival to date.

Of the entries received, approximately 100 films are chosen to compete in a variety of categories. Films not chosen for competition still have the opportunity to be seen during the festival by the industry's leaders. An additional 100 films are shown out of competition in showcase screenings.

Categories continue to evolve in order to reflect the ever-changing nature of animation. In recent years, the festival has shifted its award category focus from celebrating the art of animation to recognizing the artistry behind both independent and commercial work. Animated features were added to awards competition during OIAF 2002. The commissioned category was expanded to include animated adult and children television work for OIAF 2004.

Founded at the dawn of computer animation, the festival continues to display the latest in animation technology, while still celebrating the variety and talent behind so-called traditional animation. From the first computer-generated animation workshop led by National Research Council scientist Nestor Burtnyk in 1976 to the expansion of the New Media category from one umbrella to four sub-categories in 2004, the festival remains on the cusp of animation's cutting-edge.

To further meet industry needs, the OIAF organized its first-ever Television Animation Conference (TAC) in 2002, a chance for Canadian and international animation producers, broadcasters, and buyers to network, discuss industry issues, and do business. The two-day annual conference is held during the festival at the prestigious Chateau Laurier Hotel in downtown Ottawa.

Overcoming an office fire in 1999, a move to Toronto in 1984, then Hamilton in 1986, and incessant government funding cuts, the Ottawa International Animation Festival has proven its resiliency and maintained its relevance for over three decades. Always popular, hundreds of guests traverse oceans and borders to attend the event.

Today's OIAF thrives, providing a much-needed forum for filmmakers, producers, and animation fans to gather and celebrate this diverse and unique art form.

Ottawa International Student Animation Festival (SAFO), introduced in 1997 and held in alternate years to the larger OIAF, was created to provide a venue for student and emerging animators to draw extra attention to their work. Children, high school, undergraduate, graduate and first-time filmmakers were provided with a distinct venue to show their films, discuss issues, and meet other young filmmakers, animation educators, and industry representatives.

When the OIAF moved from a biennial to an annual festival in 2005, the student categories become a part of the main festival. The OIAF is committed to ensuring the animation profession benefits from exposure to outstanding creativity and originality of emerging work, and young animators gain access to the movers and shakers of their chosen profession.