diff --git a/packages/@ember/-internals/glimmer/lib/helpers/-in-element-null-check.ts b/packages/@ember/-internals/glimmer/lib/helpers/-in-element-null-check.ts
new file mode 100644
index 00000000000..26b5340443e
--- /dev/null
+++ b/packages/@ember/-internals/glimmer/lib/helpers/-in-element-null-check.ts
@@ -0,0 +1,38 @@
+import { assert } from '@ember/debug';
+import { DEBUG } from '@glimmer/env';
+import { Helper, VMArguments } from '@glimmer/interfaces';
+import { VersionedPathReference } from '@glimmer/reference';
+import { Tag } from '@glimmer/validator';
+
+let helper: Helper;
+
+if (DEBUG) {
+  class InElementNullCheckReference implements VersionedPathReference {
+    public tag: Tag;
+
+    constructor(private inner: VersionedPathReference) {
+      this.tag = inner.tag;
+    }
+
+    value(): unknown {
+      let value = this.inner.value();
+
+      assert(
+        'You cannot pass a null or undefined destination element to in-element',
+        value !== null && value !== undefined
+      );
+
+      return value;
+    }
+
+    get(key: string): VersionedPathReference {
+      return this.inner.get(key);
+    }
+  }
+
+  helper = (args: VMArguments) => new InElementNullCheckReference(args.positional.at(0));
+} else {
+  helper = (args: VMArguments) => args.positional.at(0);
+}
+
+export default helper;
diff --git a/packages/@ember/-internals/glimmer/lib/resolver.ts b/packages/@ember/-internals/glimmer/lib/resolver.ts
index 90fdedbad1e..3550593bd7c 100644
--- a/packages/@ember/-internals/glimmer/lib/resolver.ts
+++ b/packages/@ember/-internals/glimmer/lib/resolver.ts
@@ -30,6 +30,7 @@ import InternalComponentManager, {
 import { TemplateOnlyComponentDefinition } from './component-managers/template-only';
 import { isClassHelper, isHelperFactory } from './helper';
 import { default as componentAssertionHelper } from './helpers/-assert-implicit-component-helper-argument';
+import { default as inElementNullCheckHelper } from './helpers/-in-element-null-check';
 import { default as normalizeClassHelper } from './helpers/-normalize-class';
 import { default as trackArray } from './helpers/-track-array';
 import { default as action } from './helpers/action';
@@ -262,6 +263,7 @@ const BUILTINS_HELPERS: IBuiltInHelpers = {
   '-mount': mountHelper,
   '-outlet': outletHelper,
   '-assert-implicit-component-helper-argument': componentAssertionHelper,
+  '-in-el-null': inElementNullCheckHelper,
 };
 
 interface IBuiltInModifiers {
diff --git a/packages/@ember/-internals/glimmer/tests/integration/syntax/public-in-element-test.js b/packages/@ember/-internals/glimmer/tests/integration/syntax/public-in-element-test.js
index 9d653c287e7..7a9a6db03be 100644
--- a/packages/@ember/-internals/glimmer/tests/integration/syntax/public-in-element-test.js
+++ b/packages/@ember/-internals/glimmer/tests/integration/syntax/public-in-element-test.js
@@ -119,6 +119,42 @@ moduleFor(
       }, /Can only pass null to insertBefore in in-element, received:/);
     }
 
+    ['@feature(EMBER_GLIMMER_IN_ELEMENT) does not allow null as a destination element']() {
+      let someElement = null;
+
+      expectAssertion(() => {
+        this.render(
+          strip`
+            {{#in-element someElement}}
+              {{text}}
+            {{/in-element}}
+          `,
+          {
+            someElement,
+            text: 'Whoop!',
+          }
+        );
+      }, /You cannot pass a null or undefined destination element to in-element/);
+    }
+
+    ['@feature(EMBER_GLIMMER_IN_ELEMENT) does not undefined as a destination element']() {
+      let someElement = undefined;
+
+      expectAssertion(() => {
+        this.render(
+          strip`
+            {{#in-element someElement}}
+              {{text}}
+            {{/in-element}}
+          `,
+          {
+            someElement,
+            text: 'Whoop!',
+          }
+        );
+      }, /You cannot pass a null or undefined destination element to in-element/);
+    }
+
     ['@feature(EMBER_GLIMMER_IN_ELEMENT) components are cleaned up properly'](assert) {
       let hooks = [];
 
diff --git a/packages/ember-template-compiler/lib/plugins/transform-in-element.ts b/packages/ember-template-compiler/lib/plugins/transform-in-element.ts
index 5c17597ccb6..9a84aed7b40 100644
--- a/packages/ember-template-compiler/lib/plugins/transform-in-element.ts
+++ b/packages/ember-template-compiler/lib/plugins/transform-in-element.ts
@@ -55,6 +55,15 @@ export default function transformInElement(env: ASTPluginEnvironment): ASTPlugin
 
         if (node.path.original === 'in-element') {
           if (EMBER_GLIMMER_IN_ELEMENT) {
+            let originalValue = node.params[0];
+
+            if (originalValue) {
+              let subExpr = b.sexpr('-in-el-null', [originalValue]);
+
+              node.params.shift();
+              node.params.unshift(subExpr);
+            }
+
             node.hash.pairs.forEach(pair => {
               if (pair.key === 'insertBefore') {
                 assert(