diff --git a/.changeset/famous-ghosts-roll.md b/.changeset/famous-ghosts-roll.md
new file mode 100644
index 0000000000..3da89ca103
--- /dev/null
+++ b/.changeset/famous-ghosts-roll.md
@@ -0,0 +1,7 @@
+---
+'@emotion/cache': patch
+'@emotion/css': patch
+'@emotion/react': patch
+---
+
+Fixed an edge case issue with incorrect rules being generated. When a context selector (`&`) was used not at the beginning of a selector (which is not valid SCSS but is allowed by the Stylis parser that we are using) within a group of selectors containing a pseudoclass then it was not replaced correctly with the current context selector.
diff --git a/packages/babel-plugin/package.json b/packages/babel-plugin/package.json
index fea2354535..de8b594f23 100644
--- a/packages/babel-plugin/package.json
+++ b/packages/babel-plugin/package.json
@@ -24,7 +24,7 @@
     "escape-string-regexp": "^4.0.0",
     "find-root": "^1.1.0",
     "source-map": "^0.5.7",
-    "stylis": "^4.0.3"
+    "stylis": "^4.0.10"
   },
   "peerDependencies": {
     "@babel/core": "^7.0.0"
diff --git a/packages/cache/package.json b/packages/cache/package.json
index 736a6f0f88..f29734c00b 100644
--- a/packages/cache/package.json
+++ b/packages/cache/package.json
@@ -19,7 +19,7 @@
     "@emotion/sheet": "^1.0.0",
     "@emotion/utils": "^1.0.0",
     "@emotion/weak-memoize": "^0.2.5",
-    "stylis": "^4.0.3"
+    "stylis": "^4.0.10"
   },
   "devDependencies": {
     "@emotion/hash": "*",
diff --git a/packages/cache/src/stylis-plugins.js b/packages/cache/src/stylis-plugins.js
index 62e5904c1f..b080e6db86 100644
--- a/packages/cache/src/stylis-plugins.js
+++ b/packages/cache/src/stylis-plugins.js
@@ -7,13 +7,37 @@ import {
   token,
   char,
   from,
-  identifier,
   peek,
-  position
+  position,
+  slice
 } from 'stylis'
 
 const last = arr => (arr.length ? arr[arr.length - 1] : null)
 
+// based on https://github.com/thysultan/stylis.js/blob/e6843c373ebcbbfade25ebcc23f540ed8508da0a/src/Tokenizer.js#L239-L244
+const identifierWithPointTracking = (begin, points, index) => {
+  let previous = 0
+  let character = 0
+
+  while (true) {
+    previous = character
+    character = peek()
+
+    // &\f
+    if (previous === 38 && character === 12) {
+      points[index] = 1
+    }
+
+    if (token(character)) {
+      break
+    }
+
+    next()
+  }
+
+  return slice(begin, position)
+}
+
 const toRules = (parsed, points) => {
   // pretend we've started with a comma
   let index = -1
@@ -30,7 +54,11 @@ const toRules = (parsed, points) => {
           // it's very unlikely for this sequence to actually appear in a different context, so we just leverage this fact here
           points[index] = 1
         }
-        parsed[index] += identifier(position - 1)
+        parsed[index] += identifierWithPointTracking(
+          position - 1,
+          points,
+          index
+        )
         break
       case 2:
         parsed[index] += delimit(character)
diff --git a/packages/css-prettifier/package.json b/packages/css-prettifier/package.json
index 10dcb73b13..78d08dba67 100644
--- a/packages/css-prettifier/package.json
+++ b/packages/css-prettifier/package.json
@@ -16,7 +16,7 @@
   "repository": "https://github.com/emotion-js/emotion/tree/main/packages/css-prettifier",
   "dependencies": {
     "@emotion/memoize": "^0.7.4",
-    "stylis": "^4.0.3"
+    "stylis": "^4.0.10"
   },
   "devDependencies": {},
   "publishConfig": {
diff --git a/packages/css/test/__snapshots__/selectivity.test.js.snap b/packages/css/test/__snapshots__/selectivity.test.js.snap
index dbdd3f969c..1fad1643f1 100644
--- a/packages/css/test/__snapshots__/selectivity.test.js.snap
+++ b/packages/css/test/__snapshots__/selectivity.test.js.snap
@@ -124,6 +124,26 @@ exports[`css media query with nested selector without declarations on root 1`] =
 }"
 `;
 
+exports[`css should allow a weird class containing & when pseudoclass appears in the selector group 1`] = `
+".css-13p6h3h:hover,
+.css-13p6h3h .t\\\\&t {
+  background: blue;
+}"
+`;
+
+exports[`css should allow for context selector being appended to an element type 1`] = `
+"a.css-ciaq1 {
+  background: blue;
+}"
+`;
+
+exports[`css should allow for context selector being appended to an element type when pseudoclass appears in the selector group 1`] = `
+".css-miigdc:hover,
+a.css-miigdc {
+  background: blue;
+}"
+`;
+
 exports[`orphaned pseudos in nested atrules 1`] = `
 "@media (max-width: 400px) {
   @supports (display: grid) {
diff --git a/packages/css/test/selectivity.test.js b/packages/css/test/selectivity.test.js
index 18586f8113..dd66dc32b0 100644
--- a/packages/css/test/selectivity.test.js
+++ b/packages/css/test/selectivity.test.js
@@ -117,6 +117,37 @@ describe('css', () => {
     `
     expect(sheet).toMatchSnapshot()
   })
+
+  // this isn't compatible with SCSS but is allowed in Stylis
+  test('should allow for context selector being appended to an element type', () => {
+    css`
+      a& {
+        background: blue;
+      }
+    `
+    expect(sheet).toMatchSnapshot()
+  })
+
+  // #2488
+  test('should allow for context selector being appended to an element type when pseudoclass appears in the selector group', () => {
+    css`
+      &:hover,
+      a& {
+        background: blue;
+      }
+    `
+    expect(sheet).toMatchSnapshot()
+  })
+
+  test('should allow a weird class containing & when pseudoclass appears in the selector group', () => {
+    css`
+      &:hover,
+      .t\\&t {
+        background: blue;
+      }
+    `
+    expect(sheet).toMatchSnapshot()
+  })
 })
 
 describe('orphaned pseudos', () => {
diff --git a/packages/jest/package.json b/packages/jest/package.json
index ba705c039b..3a7bd14762 100644
--- a/packages/jest/package.json
+++ b/packages/jest/package.json
@@ -21,7 +21,7 @@
     "@emotion/css-prettifier": "^1.0.0",
     "chalk": "^4.1.0",
     "specificity": "^0.4.1",
-    "stylis": "^4.0.3"
+    "stylis": "^4.0.10"
   },
   "peerDependencies": {
     "@types/jest": "^26.0.14",
diff --git a/yarn.lock b/yarn.lock
index 6a8f6fe8df..e841eb4cc6 100644
--- a/yarn.lock
+++ b/yarn.lock
@@ -26417,10 +26417,10 @@ stylehacks@^4.0.0:
     postcss "^7.0.0"
     postcss-selector-parser "^3.0.0"
 
-stylis@^4.0.3:
-  version "4.0.3"
-  resolved "https://registry.yarnpkg.com/stylis/-/stylis-4.0.3.tgz#0d714765f3f694a685550f0c45411ebf90a9bded"
-  integrity sha512-iAxdFyR9cHKp4H5M2dJlDnvcb/3TvPprzlKjvYVbH7Sh+y8hjY/mUu/ssdcvVz6Z4lKI3vsoS0jAkMYmX7ozfA==
+stylis@^4.0.10:
+  version "4.0.10"
+  resolved "https://registry.yarnpkg.com/stylis/-/stylis-4.0.10.tgz#446512d1097197ab3f02fb3c258358c3f7a14240"
+  integrity sha512-m3k+dk7QeJw660eIKRRn3xPF6uuvHs/FFzjX3HQ5ove0qYsiygoAhwn5a3IYKaZPo5LrYD0rfVmtv1gNY1uYwg==
 
 sudo-prompt@^8.2.0:
   version "8.2.5"