diff --git a/cms/djangoapps/contentstore/models.py b/cms/djangoapps/contentstore/models.py
index 9baa3799ed..0685b93f02 100644
--- a/cms/djangoapps/contentstore/models.py
+++ b/cms/djangoapps/contentstore/models.py
@@ -97,9 +97,9 @@ class EntityLinkBase(models.Model):
     )
     # A downstream entity can only link to single upstream entity
     # whereas an entity can be upstream for multiple downstream entities.
-    downstream_usage_key = UsageKeyField(max_length=255, unique=True)
+    downstream_usage_key = UsageKeyField(unique=True)
     # Search by course/downstream key
-    downstream_context_key = CourseKeyField(max_length=255, db_index=True)
+    downstream_context_key = CourseKeyField(db_index=True)
     # This is present if the creation of this link is a consequence of
     # importing a container that has one or more levels of children.
     # This represents the parent (container) in the top level
@@ -152,7 +152,6 @@ class ComponentLink(EntityLinkBase):
         blank=True,
     )
     upstream_usage_key = UsageKeyField(
-        max_length=255,
         help_text=_(
             "Upstream block usage key, this value cannot be null"
             " and useful to track upstream library blocks that do not exist yet"
@@ -324,7 +323,6 @@ class ContainerLink(EntityLinkBase):
         blank=True,
     )
     upstream_container_key = ContainerKeyField(
-        max_length=255,
         help_text=_(
             "Upstream block key (e.g. lct:...), this value cannot be null "
             "and is useful to track upstream library blocks that do not exist yet "
@@ -564,7 +562,6 @@ class LearningContextLinksStatus(models.Model):
     course or a learning context.
     """
     context_key = CourseKeyField(
-        max_length=255,
         # Single entry for a learning context or course
         unique=True,
         help_text=_("Linking status for course context key"),
diff --git a/cms/djangoapps/modulestore_migrator/migrations/0008_key_case_sensitive.py b/cms/djangoapps/modulestore_migrator/migrations/0008_key_case_sensitive.py
new file mode 100644
index 0000000000..49dbc90140
--- /dev/null
+++ b/cms/djangoapps/modulestore_migrator/migrations/0008_key_case_sensitive.py
@@ -0,0 +1,33 @@
+# Generated by Django 5.2.11 on 2026-02-23 23:41
+
+import opaque_keys.edx.django.models
+from django.db import migrations
+
+
+class Migration(migrations.Migration):
+    dependencies = [
+        ("modulestore_migrator", "0001_squashed_0007_switch_to_openedx_content"),
+    ]
+
+    operations = [
+        migrations.AlterField(
+            model_name="modulestoreblocksource",
+            name="key",
+            field=opaque_keys.edx.django.models.UsageKeyField(
+                case_sensitive=True,
+                help_text="Original usage key of the XBlock that has been imported.",
+                max_length=255,
+                unique=True,
+            ),
+        ),
+        migrations.AlterField(
+            model_name="modulestoresource",
+            name="key",
+            field=opaque_keys.edx.django.models.LearningContextKeyField(
+                case_sensitive=True,
+                help_text="Key of the content source (a course or a legacy library)",
+                max_length=255,
+                unique=True,
+            ),
+        ),
+    ]
diff --git a/cms/djangoapps/modulestore_migrator/models.py b/cms/djangoapps/modulestore_migrator/models.py
index 17da8e1870..6571a28137 100644
--- a/cms/djangoapps/modulestore_migrator/models.py
+++ b/cms/djangoapps/modulestore_migrator/models.py
@@ -47,8 +47,8 @@ class ModulestoreSource(models.Model):
       control whether `forwarded` is set to any given migration.
     """
     key = LearningContextKeyField(
-        max_length=255,
         unique=True,
+        case_sensitive=True,
         help_text=_('Key of the content source (a course or a legacy library)'),
     )
     forwarded = models.OneToOneField(
@@ -189,7 +189,7 @@ class ModulestoreBlockSource(TimeStampedModel):
         related_name="blocks",
     )
     key = UsageKeyField(
-        max_length=255,
+        case_sensitive=True,
         unique=True,
         help_text=_('Original usage key of the XBlock that has been imported.'),
     )
diff --git a/common/djangoapps/course_modes/models.py b/common/djangoapps/course_modes/models.py
index 2e711a1081..a739a9076f 100644
--- a/common/djangoapps/course_modes/models.py
+++ b/common/djangoapps/course_modes/models.py
@@ -943,7 +943,7 @@ class CourseModesArchive(models.Model):
         app_label = "course_modes"
 
     # the course that this mode is attached to
-    course_id = CourseKeyField(max_length=255, db_index=True)
+    course_id = CourseKeyField(db_index=True)
 
     # the reference to this mode that can be used by Enrollments to generate
     # similar behavior for the same slug across courses
diff --git a/common/djangoapps/status/models.py b/common/djangoapps/status/models.py
index 2d37faedb8..6685643432 100644
--- a/common/djangoapps/status/models.py
+++ b/common/djangoapps/status/models.py
@@ -64,7 +64,7 @@ class CourseMessage(models.Model):
     .. no_pii:
     """
     global_message = models.ForeignKey(GlobalStatusMessage, on_delete=models.CASCADE)
-    course_key = CourseKeyField(max_length=255, blank=True, db_index=True)
+    course_key = CourseKeyField(blank=True, db_index=True)
     message = models.TextField(blank=True, null=True)
 
     def __str__(self):
diff --git a/common/djangoapps/student/models/user.py b/common/djangoapps/student/models/user.py
index 8d10db4b0f..a9055d5247 100644
--- a/common/djangoapps/student/models/user.py
+++ b/common/djangoapps/student/models/user.py
@@ -93,7 +93,7 @@ class AnonymousUserId(models.Model):
 
     user = models.ForeignKey(User, db_index=True, on_delete=models.CASCADE)
     anonymous_user_id = models.CharField(unique=True, max_length=32)
-    course_id = LearningContextKeyField(db_index=True, max_length=255, blank=True)
+    course_id = LearningContextKeyField(db_index=True, blank=True)
 
 
 def anonymous_id_for_user(user, course_id):
@@ -1058,7 +1058,7 @@ class CourseAccessRole(models.Model):
     # blank org is for global group based roles such as course creator (may be deprecated)
     org = models.CharField(max_length=64, db_index=True, blank=True)
     # blank course_id implies org wide role
-    course_id = CourseKeyField(max_length=255, db_index=True, blank=True)
+    course_id = CourseKeyField(db_index=True, blank=True)
     role = models.CharField(max_length=64, db_index=True)
 
     class Meta:
@@ -1116,7 +1116,7 @@ class CourseAccessRoleHistory(TimeStampedModel):
 
     user = models.ForeignKey(User, on_delete=models.CASCADE)
     org = models.CharField(max_length=64, db_index=True, blank=True)
-    course_id = CourseKeyField(max_length=255, db_index=True, blank=True)
+    course_id = CourseKeyField(db_index=True, blank=True)
     role = models.CharField(max_length=64, db_index=True)
     action_type = models.CharField(max_length=10, choices=ACTION_CHOICES, db_index=True)
     changed_by = models.ForeignKey(
@@ -1493,7 +1493,7 @@ class EntranceExamConfiguration(models.Model):
     """
 
     user = models.ForeignKey(User, db_index=True, on_delete=models.CASCADE)
-    course_id = CourseKeyField(max_length=255, db_index=True)
+    course_id = CourseKeyField(db_index=True)
     created = models.DateTimeField(auto_now_add=True, null=True, db_index=True)
     updated = models.DateTimeField(auto_now=True, db_index=True)
 
diff --git a/lms/djangoapps/bulk_email/models.py b/lms/djangoapps/bulk_email/models.py
index b1a7aa5744..4ee71be039 100644
--- a/lms/djangoapps/bulk_email/models.py
+++ b/lms/djangoapps/bulk_email/models.py
@@ -255,7 +255,7 @@ class CourseEmail(Email):
     class Meta:
         app_label = "bulk_email"
 
-    course_id = CourseKeyField(max_length=255, db_index=True)
+    course_id = CourseKeyField(db_index=True)
     # to_option is deprecated and unused, but dropping db columns is hard so it's still here for legacy reasons
     to_option = models.CharField(max_length=64, choices=[("deprecated", "deprecated")])
     targets = models.ManyToManyField(Target)
@@ -314,7 +314,7 @@ class Optout(models.Model):
     # We need to first create the 'user' column with some sort of default in order to run the data migration,
     # and given the unique index, 'null' is the best default value.
     user = models.ForeignKey(User, db_index=True, null=True, on_delete=models.CASCADE)
-    course_id = CourseKeyField(max_length=255, db_index=True)
+    course_id = CourseKeyField(db_index=True)
 
     class Meta:
         app_label = "bulk_email"
@@ -430,7 +430,7 @@ class CourseAuthorization(models.Model):
         app_label = "bulk_email"
 
     # The course that these features are attached to.
-    course_id = CourseKeyField(max_length=255, db_index=True, unique=True)
+    course_id = CourseKeyField(db_index=True, unique=True)
 
     # Whether or not to enable instructor email
     email_enabled = models.BooleanField(default=False)
@@ -462,7 +462,7 @@ class DisabledCourse(models.Model):
     class Meta:
         app_label = "bulk_email"
 
-    course_id = CourseKeyField(max_length=255, db_index=True, unique=True)
+    course_id = CourseKeyField(db_index=True, unique=True)
 
     @classmethod
     def instructor_email_disabled_for_course(cls, course_id):
diff --git a/lms/djangoapps/ccx/models.py b/lms/djangoapps/ccx/models.py
index 21f0136f07..7341922cec 100644
--- a/lms/djangoapps/ccx/models.py
+++ b/lms/djangoapps/ccx/models.py
@@ -26,7 +26,7 @@ class CustomCourseForEdX(models.Model):
 
     .. no_pii:
     """
-    course_id = CourseKeyField(max_length=255, db_index=True)
+    course_id = CourseKeyField(db_index=True)
     display_name = models.CharField(max_length=255)
     coach = models.ForeignKey(User, db_index=True, on_delete=models.CASCADE)
     # if not empty, this field contains a json serialized list of
@@ -112,7 +112,7 @@ class CcxFieldOverride(models.Model):
     .. no_pii:
     """
     ccx = models.ForeignKey(CustomCourseForEdX, db_index=True, on_delete=models.CASCADE)
-    location = UsageKeyField(max_length=255, db_index=True)
+    location = UsageKeyField(db_index=True)
     field = models.CharField(max_length=255)
 
     class Meta:
diff --git a/lms/djangoapps/certificates/models.py b/lms/djangoapps/certificates/models.py
index ac674167a2..985e4ea6ea 100644
--- a/lms/djangoapps/certificates/models.py
+++ b/lms/djangoapps/certificates/models.py
@@ -60,7 +60,7 @@ class CertificateAllowlist(TimeStampedModel):
     objects = NoneToEmptyManager()
 
     user = models.ForeignKey(User, on_delete=models.CASCADE)
-    course_id = CourseKeyField(max_length=255, blank=True, default=None)
+    course_id = CourseKeyField(blank=True, default=None)
     allowlist = models.BooleanField(default=0)
     notes = models.TextField(default=None, null=True)
 
@@ -219,7 +219,7 @@ class GeneratedCertificate(models.Model):
     ]
 
     user = models.ForeignKey(User, on_delete=models.CASCADE)
-    course_id = CourseKeyField(max_length=255, blank=True, default=None)
+    course_id = CourseKeyField(blank=True, default=None)
     verify_uuid = models.CharField(max_length=32, blank=True, default='', db_index=True)
     grade = models.CharField(max_length=5, blank=True, default='')
     key = models.CharField(max_length=32, blank=True, default='')
@@ -554,7 +554,7 @@ class CertificateGenerationHistory(TimeStampedModel):
     .. no_pii:
     """
 
-    course_id = CourseKeyField(max_length=255)
+    course_id = CourseKeyField()
     generated_by = models.ForeignKey(User, on_delete=models.CASCADE)
     instructor_task = models.ForeignKey(InstructorTask, on_delete=models.CASCADE)
     is_regeneration = models.BooleanField(default=False)
@@ -714,7 +714,7 @@ class ExampleCertificateSet(TimeStampedModel):
 
     .. no_pii:
     """
-    course_key = CourseKeyField(max_length=255, db_index=True)
+    course_key = CourseKeyField(db_index=True)
 
     class Meta:
         get_latest_by = 'created'
@@ -975,7 +975,7 @@ class CertificateGenerationCourseSetting(TimeStampedModel):
 
     .. no_pii:
     """
-    course_key = CourseKeyField(max_length=255, db_index=True)
+    course_key = CourseKeyField(db_index=True)
 
     self_generation_enabled = models.BooleanField(
         default=False,
diff --git a/lms/djangoapps/course_api/tests/test_views.py b/lms/djangoapps/course_api/tests/test_views.py
index d0f50c5818..2839b21c4c 100644
--- a/lms/djangoapps/course_api/tests/test_views.py
+++ b/lms/djangoapps/course_api/tests/test_views.py
@@ -446,8 +446,8 @@ class CourseListSearchViewTest(CourseApiTestViewMixin, ModuleStoreTestCase, Sear
         self.setup_user(self.audit_user)
 
         # These query counts were found empirically
-        query_counts = [52, 46, 46, 46, 46, 46, 46, 46, 46, 46, 16]
-        ordered_course_ids = sorted([str(cid) for cid in (course_ids + [c.id for c in self.courses])])
+        query_counts = [57, 46, 46, 46, 46, 46, 46, 46, 46, 43, 12]
+        ordered_course_ids = sorted([str(cid) for cid in (course_ids + [c.id for c in self.courses])], key=str.lower)
 
         self.clear_caches()
 
diff --git a/lms/djangoapps/lti_provider/models.py b/lms/djangoapps/lti_provider/models.py
index f763321748..621d2bb8d1 100644
--- a/lms/djangoapps/lti_provider/models.py
+++ b/lms/djangoapps/lti_provider/models.py
@@ -129,8 +129,8 @@ class GradedAssignment(models.Model):
     .. no_pii:
     """
     user = models.ForeignKey(User, db_index=True, on_delete=models.CASCADE)
-    course_key = CourseKeyField(max_length=255, db_index=True)
-    usage_key = UsageKeyField(max_length=255, db_index=True)
+    course_key = CourseKeyField(db_index=True)
+    usage_key = UsageKeyField(db_index=True)
     outcome_service = models.ForeignKey(OutcomeService, on_delete=models.CASCADE)
     lis_result_sourcedid = models.CharField(max_length=255, db_index=True)
     version_number = models.IntegerField(default=0)
diff --git a/lms/djangoapps/program_enrollments/models.py b/lms/djangoapps/program_enrollments/models.py
index 2abec16d93..b837c26e59 100644
--- a/lms/djangoapps/program_enrollments/models.py
+++ b/lms/djangoapps/program_enrollments/models.py
@@ -128,7 +128,7 @@ class ProgramCourseEnrollment(TimeStampedModel):
         blank=True,
         on_delete=models.CASCADE
     )
-    course_key = CourseKeyField(max_length=255)
+    course_key = CourseKeyField()
     status = models.CharField(max_length=9, choices=STATUS_CHOICES)
     historical_records = HistoricalRecords()
 
diff --git a/lms/djangoapps/support/models.py b/lms/djangoapps/support/models.py
index d8f6e2b9a1..99dca53937 100644
--- a/lms/djangoapps/support/models.py
+++ b/lms/djangoapps/support/models.py
@@ -24,7 +24,7 @@ class CourseResetCourseOptIn(TimeStampedModel):
 
     .. no_pii:
     """
-    course_id = CourseKeyField(max_length=255, unique=True)
+    course_id = CourseKeyField(unique=True)
     active = BooleanField()
 
     def __str__(self):
diff --git a/lms/djangoapps/teams/models.py b/lms/djangoapps/teams/models.py
index d58fe9801d..ff53871f22 100644
--- a/lms/djangoapps/teams/models.py
+++ b/lms/djangoapps/teams/models.py
@@ -130,7 +130,7 @@ class CourseTeam(models.Model):
     team_id = models.SlugField(max_length=255, unique=True)
     discussion_topic_id = models.SlugField(max_length=255, unique=True)
     name = models.CharField(max_length=255, db_index=True)
-    course_id = CourseKeyField(max_length=255, db_index=True)
+    course_id = CourseKeyField(db_index=True)
     topic_id = models.CharField(default='', max_length=255, db_index=True, blank=True)
     date_created = models.DateTimeField(auto_now_add=True)
     description = models.CharField(max_length=300)
diff --git a/lms/djangoapps/verify_student/models.py b/lms/djangoapps/verify_student/models.py
index cee18ca8d3..2c9edf9b6d 100644
--- a/lms/djangoapps/verify_student/models.py
+++ b/lms/djangoapps/verify_student/models.py
@@ -1091,7 +1091,6 @@ class VerificationDeadline(TimeStampedModel):
         app_label = "verify_student"
 
     course_key = CourseKeyField(
-        max_length=255,
         db_index=True,
         unique=True,
         help_text=gettext_lazy("The course for which this deadline applies"),
diff --git a/requirements/edx/base.txt b/requirements/edx/base.txt
index 99b34b47b2..05c9a594b7 100644
--- a/requirements/edx/base.txt
+++ b/requirements/edx/base.txt
@@ -485,7 +485,7 @@ edx-i18n-tools==1.9.0
     #   xblocks-contrib
 edx-milestones==1.1.0
     # via -r requirements/edx/kernel.in
-edx-opaque-keys[django]==3.0.0
+edx-opaque-keys[django]==3.1.0
     # via
     #   -r requirements/edx/kernel.in
     #   edx-bulk-grades
diff --git a/requirements/edx/development.txt b/requirements/edx/development.txt
index e176170e9c..8e3f7bb879 100644
--- a/requirements/edx/development.txt
+++ b/requirements/edx/development.txt
@@ -777,7 +777,7 @@ edx-milestones==1.1.0
     # via
     #   -r requirements/edx/doc.txt
     #   -r requirements/edx/testing.txt
-edx-opaque-keys[django]==3.0.0
+edx-opaque-keys[django]==3.1.0
     # via
     #   -r requirements/edx/doc.txt
     #   -r requirements/edx/testing.txt
diff --git a/requirements/edx/doc.txt b/requirements/edx/doc.txt
index 48e5eac571..e46f772e58 100644
--- a/requirements/edx/doc.txt
+++ b/requirements/edx/doc.txt
@@ -574,7 +574,7 @@ edx-i18n-tools==1.9.0
     #   xblocks-contrib
 edx-milestones==1.1.0
     # via -r requirements/edx/base.txt
-edx-opaque-keys[django]==3.0.0
+edx-opaque-keys[django]==3.1.0
     # via
     #   -r requirements/edx/base.txt
     #   edx-bulk-grades
diff --git a/requirements/edx/testing.txt b/requirements/edx/testing.txt
index ee113180e3..6cb004cc17 100644
--- a/requirements/edx/testing.txt
+++ b/requirements/edx/testing.txt
@@ -598,7 +598,7 @@ edx-lint==5.6.0
     # via -r requirements/edx/testing.in
 edx-milestones==1.1.0
     # via -r requirements/edx/base.txt
-edx-opaque-keys[django]==3.0.0
+edx-opaque-keys[django]==3.1.0
     # via
     #   -r requirements/edx/base.txt
     #   edx-bulk-grades