While the gameplay remains unchanged for all of the classic titles offered for the Virtual Console, Nintendo has stated that some games may be improved with sharper graphics or better frame rates. Certainly, many PAL SNES games run with significantly reduced borders compared to the original cartridge releases. As with disc-based games, the Virtual Console service is region-locked — that is, different versions of games are provided to different regions, and game availability may vary from region to region.

Nintendo had stated that the Wii Shop Channel would not be used exclusively for retro games, and WiiWare games have appeared in North America as of May 12, 2008. These original games are made available through the WiiWare part of the Wii Shop Channel, as opposed to through the Virtual Console.

Satoru Iwata stated in a speech on March 23, 2006, that Nintendo, Sega, and Hudson Soft were working in collaboration to bring a "best of" series of games to the Wii. At the following E3, Hudson also declared it would bring upwards of 100 titles to the Wii's Virtual Console. Additionally, Hudson mentioned that its lawyers were working on acquiring the licenses to games from now defunct companies. Nintendo announced MSX compatibility on September 19, 2006, announcing on February 23, 2007 that the MSX titles Eggy and Aleste would be released in Japan. In February 2007, a heading for Neo Geo games was added to the Japanese Virtual Console page, and in September of that same year, games for that system appeared on the list of future releases, priced at 900 points each. Also in September Hudson announced that games made for the TurboGrafx-CD format would also join the Virtual Console beginning in October 2007, with five titles to be released for the remainder of 2007 and ten titles for 2008. They will be priced at 800 points.

On June 1, 2007, Nintendo of America issued a press release to announce the upcoming release of its 100th Virtual Console title, which was Zelda II: The Adventure of Link. Within this press release, Nintendo stated that more than 4.7 million Virtual Console games had been downloaded, at a rate of more than 1,000 titles an hour.

Neo Geo support was added on September 18, 2007 for the Japanese Virtual Console, becoming the first addition to the list of consoles since the TurboGrafx-16 was added two days after the U.S. launch.

On October 9, 2007, Nintendo announced that 7.8 million Virtual Console titles had been downloaded, and as of December 2007, this number topped ten million.

Games from several new past consoles were added during 2008: Sega Master System on February 26, 2008 for Japan's Virtual Console, with other regions and Game Gear support under the Master System label to follow at currently unknown times; Commodore 64 support was added on March 28, 2008 for Europe's Virtual Console. and MSX support was added on May 27, 2008 for Japan's Virtual Console.

On February 23, 2009, the first 3 Commodore 64 titles (International Karate, The Last Ninja and Pitstop II) were added to the North America Virtual Console for the first time.

On March 25, 2009, simultaneously with Nintendo's Keynote Speech at Game Developers Conference, Nintendo launched 'Virtual Console Arcade', launching with four titles, Mappy, The Tower of Druaga, Star Force and Gaplus.

The Wii Shop Channel has functionality to allow games to be updated. This has been used four times so far to update Military Madness, Star Fox 64/Lylat Wars, Kirby 64: The Crystal Shards (in North America and Europe), and Mario Kart 64 (in Europe and Australia). Several NES and SNES games released before March 30, 2007 have also been given updates in Europe and Australia to fix previous problems with the Wii component cables. These updates are free of charge to those who have downloaded a previous version of the game.