Collins says she will not let up questioning the Government and its plans for partnership with Māori.
The exchange sparked a debate on whether MPs should be allowed to call each other racist in the House, with the Speaker ruling policies and views could be labelled racist but not MPs.
"It's been accumulating over the last couple of weeks, Waititi told Morning Report.
"It's hard to explain unless you are Māori and you can feel this barrage of racist rhetoric towards Māori."
"It's not just the He Puapua report, it's around Māori wards, it's around the Māori Health Authority, and all of these kaupapa which are equitable for Māori.
"What it is doing is inciting a whole lot of racists to come out on social media with venom, with absolute venom.
"We will not stand for it, it's unacceptable."
National was down in the polls and was often using tangata whenua and Māori as a political football to gain popularity, he said.
"When National talked about Māori wards being apartheid, about the Māori Health Authority being separatist and now they're talking about the He Puapua report also being apartheid and separatist - they can use words like that in Parliament, when we question them we get kicked out.
"Hence the haka yesterday because that is our way of debating issues."
Waititi said it was time to have "a mature conversation in this country about how we do politics".
"Māori are sick and tired of being the political football," he said.
Waititi said if he had to learn how to frame his questions properly so should Collins.
National Party deputy leader Shane Reti said National's questions in Parliament were legitimate, and he supported Judith Collins.
Reti said questions in Parliament before Waititi raised a point of order were reasonable and legitimate on He Puapua and the dual Government.
"For Rawiri to say that line of questioning is racist ... no, that is an inquiring line of questioning raising clarification, trying to get some understanding of what's not part of current public discussion.
"Yes I agree tone is important ... and yes I do support Judith in the constructive way in which she is looking to bring this discussion forward."
Reti said in recent speeches Collins had identified that National sees the Treaty of Waitangi as the founding document and there had been breaches which settlements sought to address. The party was also discussing having a Treaty clause placed back in its constitution.
Asked how a wider discussion on Treaty issues could take place without many tangata whenua feeling as though there is a backlash because of language used by Judith Collins, Reti said:
"We can only control the composure we think needs to be out there to have that discussion. If others feel we haven't got that tone right then we can certainly look to see how we can do it better.
"But we're not the Government of the day and the prime setters of those parameters. We think the Government should be setting this discussion piece - we'll contribute to that discussion."
National was still pondering Speaker Trevor Mallard's ruling, he said.
"We'll have to have a caucus discussion around the issues that Trevor raised around holding racist views but not being a racist yourself and whether one can challenge policy on racist positions - those are discussions we'll need to have. I'm not going to pre-empt the views of caucus ... we'll have a deep and thoughtful discussion on this and reply to the Speaker as he's requested us to."
Waititi said a national conversation on Te Tiriti o Waitangi must include Māori.
"If we want to have a national and a mature conversation about what the Tiriti o Waitangi actually is, and I commend the comments of the Prime Minister yesterday, we're prepared to have that."
