Ardern said she did not respond directly to Handley's text message to her about the CTO role.
To the best of her recollection she had received one text about the CTO role from Handley. She had in fact received two - on April 23 and August 20.
"He mentioned the role, I didn't reply to that. I haven't replied to a text message from him since April," she said.
"He sent me a text that I did not reply to. Again, I've always said that I did not engage with him directly on the issue of the CTO role."
Asked about a text in which she said " I'll talk to the team about how we can make use of you and your kind offer" in relation to Handley's return to New Zealand, Ardern said: "He said he wanted to come back to New Zealand and get involved.
"At that point I had no idea he was at all interested in the CTO role. That is why I did not engage with him from the moment he mentioned it, it would not have been appropriate."
Ardern denied she had misled Parliament, saying there was only one text message and one email that related to the CTO role.
She would not move to clarify the parliamentary record: "I believe that I have been absolutely accurate in my description of our engagement."
The Prime Minister acknowledged that she had known Handley for a number of years.
"Enough to know that it wouldn't have been appropriate for me to engage with him when he mentioned the CTO role."
Ardern said all her communications would be released through the Official Information Act. "At the time I answered those questions I had that in mind as well."
Ardern said it would now been appropriate for someone, probably Minister Megan Woods, to get in touch with Handley to explain the process - and apologise.
What Ardern told Parliament
In response to questions from National leader Simon Bridges on August 19, Ardern told Parliament that in addition to a text message, she also received an unsolicited email to her private account from Handley on June 7 but did not open it or reply to it.
Her staff told her it had informed her he had applied for the CTO role.
In Parliament on August 18, Ardern said she had received a text message from Handley about the CTO role but said she never spoke to him.
She did not directly engage with him because it would have been inappropriate.
"My recollection is that he mentioned the CTO role, that it had been mentioned to him."
Asked whether there were any other text messages, Ardern said: "I did not directly reply to that text message on that day or engage with him on the CTO role. On the CTO role I did not engage with Mr Handley via text message."
Derek Handley releases texts, emails
Handley told the Herald today that no one from the Government has told him why he was dropped as New Zealand's chief technology officer after he'd accepted the job.
In the face of persistent questions, speculation and innuendo over the recruitment, Handley sat on the sidelines and says he was waiting for the Government to clear things up.
Handley is today releasing his messages with Ardern and Curran to "clear the air" and says it clearly shows "there was nothing untoward or inappropriate" in them.
He was offered the role but it was subsequently scrapped. Handley will be paid $107,000 in compensation and plans to give the money to charity.
Handley, who was born in Hong Kong but grew up in New Zealand, has spent the better part of a decade living in New York.
He is perhaps best known for co-founding mobile marketing business The Hyperfactory, which was sold in 2009 for a multimillion-dollar sum.
While Handley and his wife had already decided to return to New Zealand, the family arrived back in the country days before finding out his contract was scrapped.
New Government Digital Services Minister Megan Woods said last week that the recruitment process was stopped while her officials reviewed the role.
Curran was removed from Cabinet by Ardern over her failure to record and disclose a meeting she held with Handley over the role in February.