Once played irregularly every few years, Bledisloe Cup matches now happen annually, and include Rugby Championship (formerly Tri Nations) fixtures between the two sides. Their World Cup fixtures do not count as Bledisloe Cup matches, which were always played in Australia or New Zealand. However, 2008 saw a Bledisloe Cup match held outside the two countries for the first time when the teams met in Hong Kong, and a 2009 Bledisloe Cup match was played in Tokyo.
Recently New Zealand has dominated the cup, winning it 11 times in a row (2003–2013).
There is some dispute as to when the first Bledisloe Cup match was played. The Australian Rugby Union (ARU) contend that the one-off 1931 match played at Eden Park was first. However, no firm evidence has been produced to support this claim, and minutes from a New Zealand union management meeting several days later record Lord Bledisloe wishing to present a cup for the All Blacks and Wallabies to play for. The New Zealand Rugby Union (NZRU) believe that the first match was when New Zealand toured Australia in 1932.
Between 1931 and 1981 it was contested irregularly in the course of rugby tours between the two countries. New Zealand won it 19 times and Australia four times in this period including in 1949 when Australia won it for the first time on New Zealand soil. The trophy itself was apparently 'lost' during this period and reportedly rediscovered in a Melbourne store room. In the years 1982 to 1995 it was contested annually, sometimes as a series of three matches (two in 1995) and other times in a single match. During these years New Zealand won it 11 times and Australia three times.
Since 1996 the cup has been contested as part of the annual Tri Nations tournament. Until 1998 the cup was contested in a three match series: the two Tri Nations matches between these sides and a third match. New Zealand won these series in 1996 and 1997, and Australia won it in 1998.
In 1996 and from 1999 through 2005, the third match was not played; during those years, Australia and New Zealand played each other twice as part of the Tri Nations for the cup. If both teams won one of these games, or if both games were drawn, the cup was retained by its current holder. The non-holder had to win the two games 2-0 or 1-0 (with a draw) to regain the Cup. A criticism of this system was that with the closeness in the level of ability between the two sides, years where each team won one game each were very common (1999, 2000, 2002, 2004) and in these years, many rugby fans felt dissatisfied with one team keeping the cup in a series tied at 1-1.
2006 saw the return of the 3-game contest for Bledisloe as the Tri Nations series was extended so that each team played each other 3 times. The 2007 Cup, however, reverted to the two-game contest because the Tri Nations was abbreviated that year to minimise interference with the teams' preparations for the World Cup.
In 2008 it was announced that the Bledisloe Cup would be contested over an unprecedented four matches, with three games played in Australia and New Zealand and a fourth and potentially deciding game in Hong Kong in an effort to promote the game in Asia (the first time Australia and New Zealand played in a third country outside the World Cup). The Hong Kong match, which drew a crowd of 39,000 to see the All Blacks (which had already clinched the Bledisloe Cup) defeat the Wallabies 19–14, proved to be a financial success for the two unions, generating a reported £5.5 million. Even before the match, the two countries' rugby federations were considering taking Cup matches to the United States and Japan in 2009 and 2010. Japan hosted a fourth Bledisloe Test Match on 31 October 2009. Each team is expected to clear at least A$3.8 million/NZ$5 million from the Tokyo match. However a 2010 fourth match was set in Hong Kong and has struggled to attract crowds. 
The three-match format for the Bledisloe Cup continued in 2012, with the first two matches taking place as part of the 2012 Rugby Championship.