That role gave Wildstein an influence that outstripped his bureaucratic title. He led efforts to give New Jersey officials more sway over authority operations. And he was seen as having unsurpassed connections to Christie's inner circle.
Now, the man who was known as the administration's eyes and ears at the Port Authority may be the public's best chance of knowing the truth behind a plan last summer to purposely create days of traffic gridlock in Fort Lee, N.J., by choking off local access to the George Washington Bridge.
Wildstein, who pushed through the closures after receiving an email from a Christie aide saying, "Time for some traffic problems in Fort Lee," has hinted in recent days that he might be willing to tell more about what the governor knew and when he knew it.
Christie and his aides have responded by portraying Wildstein as a duplicitous rogue.
"Bottom line - David Wildstein will do and say anything to save David Wildstein," Christie's spokesman, Colin Reed, wrote in a memo distributed to the governor's supporters and some journalists.
That break marks an abrupt reversal for an administration that defended Wildstein for years, even in the face of public and private criticism that he was over-politicizing the Port Authority, intimidating the staff and meddling in operations he didn't oversee.
Wildstein, 52, joined the Port Authority as part of a wave of people with political ties who swelled its ranks shortly after Christie took office.
At the time, he had no background in transportation or public works. His previous job had been as the anonymous political blogger, known as Wally Edge, behind the influential website PolitickerNJ.
Under his leadership, the site became known for nonpartisan scoops on New Jersey political news. A former reporter there, Brian Murphy, said in an piece on the blog Talking Points Memo that Wildstein was "a fiercely loyal editor and advocate" - albeit one he never actually met. Wildstein was so secretive, even his employees didn't know his identity.
Even as he ran the site, Wildstein worked as a Republican operative, following a love of rough-and-tumble politics dating back to his days as a high school classmate of Christie's in Livingston, N.J.
While still a student, Wildstein ran for a spot on the local school board - a campaign marred by a teacher's accusation that the teenager had tricked him into signing an endorsement letter published in the town newspaper. In the mid-1980s, he had a stint on the Livingston town council and served a year as its mayor.
Christie now says the two barely knew each other.
"David and I were not friends in high school," Christie said in a news conference Jan. 9. "We didn't travel in the same circles in high school. You know, I was the class president and athlete. I don't know what David was doing during that period of time ... We went 23 years without seeing each other. And in the years we did see each other, we passed in the hallways."
At the Port Authority, Wildstein became a central figure in a revived power struggle between people installed by the Christie administration and officials who reported back to the governor of New York.
More than once, officials on the New York side complained to their New Jersey counterparts that Wildstein was bullying employees and exercising an outsized degree of control over people he didn't directly supervise.
The authority's manager of the George Washington Bridge, Robert Durando, later told a legislative committee it was Wildstein's reputation and perceived connections that kept him from asking too many questions when he was given an order to restrict access to the span from Fort Lee - and do it without telling any local authorities what was about to happen.
"I was concerned about what Mr. Wildstein's reaction would be if I did not follow his directive," Durando said.
When a Bergen County newspaper, The Record, wrote a profile of Wildstein in 2012 that noted the criticism and questioned whether he was using the agency to further a political agenda, Christie administration officials were fiercely supportive.
"He is there in that job because he is well suited to the task of playing a role in reforming the Port Authority in accordance with the governor's goals," Christie's spokesman, Michael Drewniak, told the newspaper. "If he's not liked for that role, and if he's accused of being zealous in that regard, then we plead guilty."
Port Authority Deputy Executive Director Bill Baroni also defended his approach.
"If there are people who have been here for decades, who don't like the fact that we have a real aggressive approach to getting these projects done, they should get used to it. Our job here is not to make friends," said Baroni, who, like Wildstein resigned from the Port Authority in December.
In their latest attack on Wildstein, Christie officials cited that very article several times as evidence that he had created a "culture of fear" at the Port Authority and now shouldn't be believed.
Christie has repeatedly denied having any knowledge of the bridge lane shutdowns until they were over, when The Wall Street Journal reported on an angry memo in which the Port Authority's executive director, Patrick Foye, assailed the closures as improper. Foye is an appointee of New York Gov. Andrew Cuomo, a Democrat.
Emails, made public as part of a legislative investigation, indicate that the plan to close access lanes to the George Washington Bridge was implemented days after a deputy chief of staff for Christie, Bridge Anne Kelly, sent the "traffic problems" message to Wildstein.
"Got it," he replied. As the streets in Fort Lee became impassable, and the borough's mayor begged Port Authority officials for help, Wildstein and other Christie loyalists traded text messages and emails mocking the situation and disparaging the mayor.
Silence on their intended motive has prevented the public from knowing what prompted that exchange.
Wildstein's attorney, Alan Zegas, didn't return messages seeking comment.