The agency is consulting on a proposal to bring in bilingual signage in some categories, such as for destinations and to highlight cycle or bus lanes.
Councillors supported more use of te reo Māori and said incorporating it into some signage would help to normalise its use as a living language.
Cr Christine Garey said it was "another mokopuna decision - a decision for generations to come".
"Let's embrace this and get on with it."
Cr David Benson-Pope said the issue had become a lightning rod for bigotry and racism.
It was spurious to suggest bilingual signage created safety risks, he said.
Cr Mandy Mayhem said bilingual signage was overdue.
During a period of questions, council chief executive Sandy Graham said proposed use of Māori before English reflected what was considered to be culturally appropriate.
Cr Brent Weatherall voted for the council's submission to the transport agency.
He was also said it was important to be respectful of people who did not yet understand Māori.
Cr Lee Vandervis, who had a recent social media post that indicated he would have voted against the council's submission, was not at the meeting.
Cr Steve Walker labelled his post a "dog whistle".
