diff --git a/_config/requestprocessors.yml b/_config/requestprocessors.yml
index abf0b6d5efa..e39b0e40db9 100644
--- a/_config/requestprocessors.yml
+++ b/_config/requestprocessors.yml
@@ -9,7 +9,6 @@ SilverStripe\Core\Injector\Injector:
         TrustedProxyMiddleware: '%$SilverStripe\Control\Middleware\TrustedProxyMiddleware'
         AllowedHostsMiddleware: '%$SilverStripe\Control\Middleware\AllowedHostsMiddleware'
         SessionMiddleware: '%$SilverStripe\Control\Middleware\SessionMiddleware'
-        FlushMiddleware: '%$SilverStripe\Control\Middleware\FlushMiddleware'
         ChangeDetectionMiddleware: '%$SilverStripe\Control\Middleware\ChangeDetectionMiddleware'
         HTTPCacheControleMiddleware: '%$SilverStripe\Control\Middleware\HTTPCacheControlMiddleware'
         CanonicalURLMiddleware: '%$SilverStripe\Control\Middleware\CanonicalURLMiddleware'
diff --git a/src/Control/Middleware/FlushMiddleware.php b/src/Control/Middleware/FlushMiddleware.php
deleted file mode 100644
index c14fd319df6..00000000000
--- a/src/Control/Middleware/FlushMiddleware.php
+++ /dev/null
@@ -1,38 +0,0 @@
-<?php
-
-namespace SilverStripe\Control\Middleware;
-
-use SilverStripe\Control\HTTPRequest;
-use SilverStripe\Core\ClassInfo;
-use SilverStripe\Core\Flushable;
-use SilverStripe\Core\Injector\Injector;
-use SilverStripe\Core\Kernel;
-use SilverStripe\Dev\Deprecation;
-
-/**
- * Triggers a call to flush() on all implementors of Flushable.
- * @deprecated 5.4.0 Will be replaced with flushing inside the Kernel directly.
- */
-class FlushMiddleware implements HTTPMiddleware
-{
-    public function __construct()
-    {
-        Deprecation::noticeWithNoReplacment('5.4.0', 'Will be replaced with flushing inside the Kernel directly.');
-    }
-
-    public function process(HTTPRequest $request, callable $delegate)
-    {
-        $kernel = Injector::inst()->get(Kernel::class);
-        if ((method_exists($kernel, 'isFlushed') && $kernel->isFlushed())) {
-            // Disable cache when flushing
-            HTTPCacheControlMiddleware::singleton()->disableCache(true);
-
-            foreach (ClassInfo::implementorsOf(Flushable::class) as $class) {
-                /** @var Flushable|string $class */
-                $class::flush();
-            }
-        }
-
-        return $delegate($request);
-    }
-}
diff --git a/src/Control/Middleware/HTTPCacheControlMiddleware.php b/src/Control/Middleware/HTTPCacheControlMiddleware.php
index c3da4f756c9..8f38305db07 100644
--- a/src/Control/Middleware/HTTPCacheControlMiddleware.php
+++ b/src/Control/Middleware/HTTPCacheControlMiddleware.php
@@ -9,6 +9,7 @@
 use SilverStripe\Core\Config\Configurable;
 use SilverStripe\Core\Injector\Injectable;
 use SilverStripe\Core\Injector\Injector;
+use SilverStripe\Core\Kernel;
 use SilverStripe\Core\Resettable;
 use SilverStripe\ORM\FieldType\DBDatetime;
 
@@ -35,6 +36,12 @@ class HTTPCacheControlMiddleware implements HTTPMiddleware, Resettable
      */
     public function process(HTTPRequest $request, callable $delegate)
     {
+        // Disable cache when flushing
+        $kernel = Injector::inst()->get(Kernel::class);
+        if ($kernel->isFlushed()) {
+            $this->disableCache(true);
+        }
+
         try {
             $response = $delegate($request);
         } catch (HTTPResponse_Exception $ex) {
diff --git a/src/Core/CoreKernel.php b/src/Core/CoreKernel.php
index ca9946f68a3..5626fd08082 100644
--- a/src/Core/CoreKernel.php
+++ b/src/Core/CoreKernel.php
@@ -52,6 +52,14 @@ public function boot($flush = false)
         $this->validateDatabase();
 
         $this->setBooted(true);
+
+        // Flush everything else that can be flushed, now that we're booted.
+        if ($flush) {
+            foreach (ClassInfo::implementorsOf(Flushable::class) as $class) {
+                /** @var Flushable|string $class */
+                $class::flush();
+            }
+        }
     }
 
     /**
diff --git a/src/Core/Flushable.php b/src/Core/Flushable.php
index 7b30d3d3224..77f7992b1d4 100644
--- a/src/Core/Flushable.php
+++ b/src/Core/Flushable.php
@@ -2,8 +2,6 @@
 
 namespace SilverStripe\Core;
 
-use SilverStripe\Control\Middleware\FlushMiddleware;
-
 /**
  * Provides an interface for classes to implement their own flushing functionality
  * whenever flush=1 is requested.
@@ -12,11 +10,9 @@ interface Flushable
 {
 
     /**
-     * This function is triggered early in the request if the "flush" query
-     * parameter has been set. Each class that implements Flushable implements
+     * This function is triggered early in the request if the kernel gets flushed.
+     * Each class that implements Flushable implements
      * this function which looks after it's own specific flushing functionality.
-     *
-     * @see FlushMiddleware
      */
     public static function flush();
 }
diff --git a/src/Forms/HTMLEditor/TinyMCECombinedGenerator.php b/src/Forms/HTMLEditor/TinyMCECombinedGenerator.php
index 0644c250eab..a9bbda3578c 100644
--- a/src/Forms/HTMLEditor/TinyMCECombinedGenerator.php
+++ b/src/Forms/HTMLEditor/TinyMCECombinedGenerator.php
@@ -237,13 +237,6 @@ public function generateFilename(TinyMCEConfig $config)
         return $url;
     }
 
-    /**
-     * This function is triggered early in the request if the "flush" query
-     * parameter has been set. Each class that implements Flushable implements
-     * this function which looks after it's own specific flushing functionality.
-     *
-     * @see FlushMiddleware
-     */
     public static function flush()
     {
         $dir = dirname(static::config()->get('filename_base') ?? '');
diff --git a/tests/php/Control/FlushMiddlewareTest.php b/tests/php/Control/FlushMiddlewareTest.php
deleted file mode 100644
index a553d14ba3f..00000000000
--- a/tests/php/Control/FlushMiddlewareTest.php
+++ /dev/null
@@ -1,26 +0,0 @@
-<?php
-
-namespace SilverStripe\Control\Tests;
-
-use SilverStripe\Core\Injector\Injector;
-use SilverStripe\Core\Kernel;
-use SilverStripe\Control\Tests\FlushMiddlewareTest\TestFlushable;
-use SilverStripe\Dev\FunctionalTest;
-
-class FlushMiddlewareTest extends FunctionalTest
-{
-    /**
-     * Assert that classes that implement flushable are called
-     */
-    public function testImplementorsAreCalled()
-    {
-        TestFlushable::$flushed = false;
-
-        Injector::inst()->get(Kernel::class)->boot(true);
-        $this->get('/');
-        $this->assertTrue(TestFlushable::$flushed);
-
-        // reset the kernel Flush flag
-        Injector::inst()->get(Kernel::class)->boot();
-    }
-}
diff --git a/tests/php/Core/KernelTest.php b/tests/php/Core/KernelTest.php
index c779f349521..afb5b37a7a7 100644
--- a/tests/php/Core/KernelTest.php
+++ b/tests/php/Core/KernelTest.php
@@ -15,6 +15,7 @@
 use ReflectionClass;
 use SilverStripe\ORM\DB;
 use ReflectionObject;
+use SilverStripe\Core\Tests\KernelTest\TestFlushable;
 
 class KernelTest extends SapphireTest
 {
@@ -85,7 +86,7 @@ public function testInvalidConfigDetection()
 
         $kernel->getConfigLoader()->getManifest();
     }
-    
+
     public function testReplicaDatabaseVarsLoaded()
     {
         // Set environment variables for a fake replica database
@@ -113,4 +114,16 @@ public function testReplicaDatabaseVarsLoaded()
             'password' => 'hi_people',
         ], $configs['replica_01']);
     }
+
+    public function testImplementorsAreCalled()
+    {
+        TestFlushable::$flushed = false;
+
+        $kernel = Injector::inst()->get(Kernel::class);
+        $kernel->boot(true);
+        $this->assertTrue(TestFlushable::$flushed);
+
+        // reset the kernel Flush flag
+        $kernel->boot();
+    }
 }
diff --git a/tests/php/Control/FlushMiddlewareTest/TestFlushable.php b/tests/php/Core/KernelTest/TestFlushable.php
similarity index 81%
rename from tests/php/Control/FlushMiddlewareTest/TestFlushable.php
rename to tests/php/Core/KernelTest/TestFlushable.php
index f1c290e1651..8b1f2d87ae5 100644
--- a/tests/php/Control/FlushMiddlewareTest/TestFlushable.php
+++ b/tests/php/Core/KernelTest/TestFlushable.php
@@ -1,6 +1,6 @@
 <?php
 
-namespace SilverStripe\Control\Tests\FlushMiddlewareTest;
+namespace SilverStripe\Core\Tests\KernelTest;
 
 use SilverStripe\Core\Flushable;
 use SilverStripe\Dev\TestOnly;