The Three Lions entered the match knowing that a victory would secure their spot at next summer's tournament in Russia, and a late Harry Kane effort saw Gareth Southgate's side collect all three points after a lacklustre performance.
There was no Dele Alli for England as the Tottenham Hotspur midfielder served a suspension for his middle-finger salute against Slovakia last time out.
Kane skippered for the Three Lions on his 22nd appearance for the national team, while Phil Jones's absence meant that there was a spot at centre-back for John Stones. Alex Oxlade-Chamberlain and Raheem Sterling also started, as did Marcus Rashford, who has been in fine form for Manchester United this season.
A positive start from England saw Rashford, Sterling and Oxlade-Chamberlain all enjoy space in wide positions, but Slovenia were quite comfortable inside the opening 15 minutes at an extremely quiet Wembley.
The visitors were also carrying a threat down the other end, with Roman Bezjak forcing Joe Hart to make a save, and Josip Ilicic having a decent penalty shout after going down under a challenge from Hart inside the England box.
Slovenia had another half-chance in the 19th minute when Ilicic delivered a stunning ball into Bezjak, but the number 14 could not make the most of the opportunity as England, who appeared to go off the boil after a positive start, survived another dangerous moment.
England's first serious opportunity of the match came in the 26th minute when Jordan Henderson found space inside the Slovenia box, but the Liverpool captain saw his effort saved by Oblak.
Rashford was comfortably England's biggest threat in the first period, and the Manchester United forward came close to making the breakthrough with a free kick in the final stages of the half, but Oblak was across to make a smart save once again.
Slovenia had the first half-chance of the second period after left-back Bojan Jokic met a deep cross from Bezjak, but Hart was on hand to collect at his near post.
Chievo attacker Valter Birsa came off the away side's bench in the 55th minute as England continued to struggle, with those inside Wembley showing their displeasure at what was another seriously lacklustre performance.
Slovenia, on the other hand, were growing in confidence as Birsa linked impressively with Bezjak and Ilicic in the final third of the field.
Rashford had a super chance to send England ahead just past the hour after racing into the Slovenia box following a swift counter-attack, but the 19-year-old's effort, which had beaten Oblak, was cleared by Rajko Rotman.
Jesse Lingard for Oxlade-Chamberlain was England's first change of the match, and the Manchester United attacker played a key role in the home side's next chance. The opportunity ultimately fell for Sterling just inside the Slovenia box, but Bostjan Cesar made a super block.
Kane then fired just wide of the post 20 minutes from time, but it did not take too long for Slovenia to gain a foothold once again.
The visitors had a wonderful chance to register in the 84th minute when substitute Tim Matavz raced into the England box, but Hart was out to make a fine stop as the on-loan West Ham United goalkeeper came up with a big moment late on.
Six additional minutes were played at the end of the 90, and England found the back of the net in the fourth of those as Kane tucked a low Walker cross into the back of the net to secure a seventh Group F victory for the Three Lions.
England will look to round off their qualification campaign in style when they travel to Lithuania on Sunday. Slovenia, meanwhile, will finish with a home game against now second-placed Scotland on the same night.