The Portuguese superstar hit the milestone in the 62nd minute, rescuing his side after they fell behind to Radja Nainggolan's stunning early strike.
Wojciech Szczesny could perhaps have done more to keep out Nainggolan's first-half effort, which put Inter on course for a win that would have boosted their top-three hopes.
But Ronaldo struck to ensure Juve, who celebrated an eighth successive Scudetto last week with a 2-1 victory over Fiorentina, dodged just a third league defeat of the campaign.
Juve were rattled by Inter's fast start to the match, falling behind inside seven minutes when Nainggolan thumped a scooped pass from Matteo Politano into the back of the net from 25 yards.
Szczesny failed to keep out the strike despite getting an arm to it, but he responded well by denying Mauro Icardi and Stefan de Vrij in the space of 20 seconds, the latter wasting a free header from six yards out.
Juve, whose only on target shot in the first half came from a Leonardo Bonucci drive in the opening minute, would have been further behind at the break had Blaise Matuidi not made a vital block to prevent Icardi firing home.
The visitors hit back just after the hour mark as Ronaldo picked out the bottom-right corner with a crisp drive after being teed up by a Miralem Pjanic backheel.
Ivan Perisic and substitute Joao Mario had shots saved in the final 10 minutes but neither team - Pjanic was kept out for Juve beforehand - found a way through in an end-to-end conclusion to the match.
What does it mean? Inter fail to tighten grip on third
The three points were there for the taking from Inter's perspective, but they had to settle for a draw.
Roma's 3-0 win over Cagliari earlier in the day means they closed to within four points of Luciano Spalletti's side, and AC Milan and Atalanta could reduce that to just two if they win their games in hand.
Ronaldo hits landmark goal
On the back of his blank against Fiorentina it looked like being another frustrating match for Ronaldo. The five-time Ballon d'Or winner fired over from 20 yards in his only sight of goal in the first half and then had a shot blocked by De Vrij early in the second. However, he found a way through after exchanging passes with Pjanic to end his wait for a 600th club goal.
Szczesny fails to make his case
There has been talk that Juve will turn to David de Gea to replace Szczesny ahead of next season. The Polish keeper hardly covered himself in glory with his attempt to keep out Nainggolan's opener, as well struck as it was, and it may speed up the process of bringing in a new high-profile number one.
Key Opta Facts
- Ronaldo has scored at least 20 goals in his last 10 top-flight campaigns.
- Massimiliano Allegri has fielded 34 different starting line-ups in the current Serie A season.
- Juve have conceded at least once in six straight games in all competitions for the first time since June 2015.
- Nainggolan has scored 14 of his 40 Serie A goals from outside the box.