The man with the most A-League games as coach under his belt parted company with cellar dwellers Wellington after six years in charge.
Having coached the most games of any A-League manager since the club's inception in 2007, Herbert - also the New Zealand national team coach - has resigned to focus his attention on the 2014 Fifa World Cup qualification campaign.
Assistant coach Chris Greenacre will take over the Phoenix for the rest of the season.
The 2012-13 season had been a particularly torrid time for Herbert, who previously led Wellington to three consecutive finals series among other impressive records.
However, with just one win from their past seven matches, the Wellington club have dropped to the bottom of table.
The timing of the decision was strange, though, with Phoenix playing their second of three matches in seven days when they host Newcastle on Wednesday.
But Herbert said the time was right for the club to head in a new direction.
"The results this year have not been what anyone would have wanted and I felt that it was time for someone else to take a fresh look at things at the club," Herbert said.
"So with the need for a fresh look, along with the fact that this year is an extremely important one for the All Whites, I felt I needed to step down as the Phoenix head coach.
"I've had a long and very successful tenure at the club and will always be proud of what I have achieved. But all good things must come to an end and it's time for new coaching blood and for me to move on to new and exciting challenges."
The Wellington franchise has languished at the bottom of the ladder in recent weeks and has come under heavy criticism from fans and media scribes for attempting to change their style of football midway through the season.
Wellington Phoenix chairman Rob Morrison said in accepting Herbert's resignation, the club is pleased that Herbert will take up the role of Technical Football Advisor to the Board.
"While the board accepted Ricki's resignation we were keen to ensure that his knowledge and expertise was not lost to the club," Morrison said.
"Ricki has an unparalleled record in the A-League. Without his contribution the Phoenix could not have had the success it has had."