With 47 needed off the last three overs, the situation was tailor made for one of the best finishers in world cricket, and Dhoni (61 not out from 34 balls), started in his usual fashion taking time to settle down before unleashing his power against the likes of Mohammed Siraj and Bhuvneshwar Kumar.
In the 18th over, the Ranchi stumper dispatched Siraj for a flat six over long-on before helping the ball over point and short third man for a four the next ball to milk 17 runs from the over.
The penultimate over witnessed a vintage Dhoni smashing two consecutive boundaries before using his bottom hand to launch Bhuvneshwar for a powerful six over long-on to reach his half century and leave Pune needing 11 from the final over.
The final over had medium pacer Siddharth Kaul going for a six in the very first ball from Manoj Tiwary (17 not out) before Dhoni finished off in style with a boundary through extra cover. Dhoni's match-winning knock was laced with five hits to the fence and three over it.
Chasing a stiff 177, Pune were off to a dismal start losing Ajinkya Rahane (2) in the fourth over before opener Rahul Tripathi (59) and skipper Steve Smith (27) rescued them with a 72-run second wicket stand in quick time.
Tripathi made full use of the life he got on 17 when Bipul Sharma put down a tough chance off medium pacer Mohammed Siraj's first ball of the match.
The 26-year-old immediately smacked Siraj out of the park the next ball before taking Siddharth Kaul to the cleaners twice in the next over as he got his half century in just 32 balls.
Smith at the other end, dispatched Bipul for two consecutive sixes as Pune looked on course before Afghanistan's teenaged leg-spinner Rashid Khan packed back the Australian after facing 21 balls with a googly knocking his off stump.
Two overs later, Tripathi, who by now had faced 41 balls and struck six boundaries and three huge sixes, was brilliantly ran out by a direct throw from Rashid, reducing the hosts to 98/3.
With 62 needed off the last five overs, the stage was set for former skipper Mahendra Singh Dhoni and English all-rounder Ben Stokes (10) to press the accelerator.
But purple cap holder Bhuvneshwar Kumar, who returned to bowl his second spell had other plans when he induced Stokes to loft one to deep midwicket which substitute Vijay Shankar latched on with ease.
In the end, it was Dhoni all the way who smashed the bowlers all around the park once he got his eye in with Bengal's Manoj Tiwary giving him company to see the team through.
Earlier, a late surge from all-rounder Moises Henriques helped Sunrisers Hyderabad post a healthy 176/3 after the visitors were put in to bat by Smith.
Pune faltered in the death overs, leaking 63 runs in the last five overs with Henriques (55 not out from 28 balls) and Deepak Hooda (19 not out from 10) taking the bowlers to the cleaners.
Sunrisers had a slowish start with skipper David Warner and his opening partner Shikhar Dhawan (30) putting on 55 runs before South African leg-spinner Imran Tahir gave Pune the first breakthrough in the form of Dhawan.
Dhawan's departure brought in the in-form New Zealand skipper Kane Williamson (21 from 14 balls), who added 29 for the second wicket with Warner before medium pacer Daniel Christian's off-cutter caught him plumb in front.
But it was the late order blows from Henriques and Hooda which helped the visitors go past the 150-run mark.
Henriques started by hitting two consecutive fours off medium pacer Shardul Thakur before meting out special treatment to Unadkat for two sixes while Hooda too used the long handle once off Unadkat for a flat six into the second tier over long-on.
The right-handed Australian brought up his half century in the final over of the innings with a four into the extra cover boundary off Thakur.
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