diff --git a/packages/api-v4/src/aglb/types.ts b/packages/api-v4/src/aglb/types.ts
index 14a541d0f1c..c6a416f7a2f 100644
--- a/packages/api-v4/src/aglb/types.ts
+++ b/packages/api-v4/src/aglb/types.ts
@@ -179,7 +179,7 @@ type CertificateType = 'ca' | 'downstream';
 export interface Certificate {
   id: number;
   label: string;
-  certificate: string;
+  certificate?: string; // Not returned for Alpha
   type: CertificateType;
 }
 
diff --git a/packages/manager/.changeset/pr-9941-upcoming-features-1701203325929.md b/packages/manager/.changeset/pr-9941-upcoming-features-1701203325929.md
new file mode 100644
index 00000000000..c3cefb0cbb6
--- /dev/null
+++ b/packages/manager/.changeset/pr-9941-upcoming-features-1701203325929.md
@@ -0,0 +1,5 @@
+---
+"@linode/manager": Upcoming Features
+---
+
+Add AGLB Configuration e2e tests, improve error handling, and improve UX ([#9941](https://github.com/linode/manager/pull/9941))
diff --git a/packages/manager/cypress/e2e/core/loadBalancers/load-balancer-configurations.spec.ts b/packages/manager/cypress/e2e/core/loadBalancers/load-balancer-configurations.spec.ts
index 126a4e1d1e3..588c9c27e17 100644
--- a/packages/manager/cypress/e2e/core/loadBalancers/load-balancer-configurations.spec.ts
+++ b/packages/manager/cypress/e2e/core/loadBalancers/load-balancer-configurations.spec.ts
@@ -18,6 +18,8 @@ import {
   mockGetLoadBalancerCertificates,
   mockGetLoadBalancerConfigurations,
   mockGetLoadBalancerRoutes,
+  mockUpdateLoadBalancerConfiguration,
+  mockUpdateLoadBalancerConfigurationError,
 } from 'support/intercepts/load-balancers';
 import { ui } from 'support/ui';
 
@@ -353,6 +355,151 @@ describe('Akamai Global Load Balancer configurations page', () => {
       }
     });
   });
+
+  describe('update', () => {
+    it('edits a HTTPS configuration', () => {
+      const configuration = configurationFactory.build({ protocol: 'https' });
+      const loadbalancer = loadbalancerFactory.build({
+        configurations: [{ id: configuration.id, label: configuration.label }],
+      });
+      const certificates = certificateFactory.buildList(3);
+      const routes = routeFactory.buildList(3);
+
+      mockGetLoadBalancer(loadbalancer).as('getLoadBalancer');
+      mockGetLoadBalancerConfigurations(loadbalancer.id, [configuration]).as(
+        'getConfigurations'
+      );
+      mockGetLoadBalancerCertificates(loadbalancer.id, certificates).as(
+        'getCertificates'
+      );
+      mockUpdateLoadBalancerConfiguration(loadbalancer.id, configuration).as(
+        'updateConfiguration'
+      );
+      mockGetLoadBalancerRoutes(loadbalancer.id, routes).as('getRoutes');
+
+      cy.visitWithLogin(
+        `/loadbalancers/${loadbalancer.id}/configurations/${configuration.id}`
+      );
+
+      cy.wait([
+        '@getFeatureFlags',
+        '@getClientStream',
+        '@getLoadBalancer',
+        '@getConfigurations',
+        '@getRoutes',
+        '@getCertificates',
+      ]);
+
+      // In edit mode, we will disable the "save" button if the user hasn't made any changes
+      ui.button
+        .findByTitle('Save Configuration')
+        .should('be.visible')
+        .should('be.disabled');
+
+      cy.findByLabelText('Configuration Label')
+        .should('be.visible')
+        .clear()
+        .type('new-label');
+
+      cy.findByLabelText('Port').should('be.visible').clear().type('444');
+
+      ui.button
+        .findByTitle('Apply More Certificates')
+        .should('be.visible')
+        .should('be.enabled')
+        .click();
+
+      ui.drawer.findByTitle('Apply Certificates').within(() => {
+        cy.findByLabelText('Host Header').type('example-1.com');
+
+        cy.findByLabelText('Certificate').click();
+
+        ui.autocompletePopper.findByTitle(certificates[1].label).click();
+
+        ui.button
+          .findByTitle('Save')
+          .should('be.visible')
+          .should('be.enabled')
+          .click();
+      });
+
+      ui.button
+        .findByTitle('Save Configuration')
+        .should('be.visible')
+        .should('be.enabled')
+        .click();
+
+      cy.wait('@updateConfiguration');
+    });
+
+    it('shows API errors when editing', () => {
+      const configuration = configurationFactory.build({ protocol: 'https' });
+      const loadbalancer = loadbalancerFactory.build({
+        configurations: [{ id: configuration.id, label: configuration.label }],
+      });
+
+      mockGetLoadBalancer(loadbalancer).as('getLoadBalancer');
+      mockGetLoadBalancerConfigurations(loadbalancer.id, [configuration]).as(
+        'getConfigurations'
+      );
+
+      const errors = [
+        { field: 'label', reason: 'Bad Label.' },
+        { field: 'port', reason: 'Port number is too high.' },
+        { field: 'protocol', reason: 'This protocol is not supported.' },
+        {
+          field: 'certificates[0].id',
+          reason: 'Certificate 0 does not exist.',
+        },
+        {
+          field: 'certificates[0].hostname',
+          reason: 'That hostname is too long.',
+        },
+        { field: 'route_ids', reason: 'Some of these routes do not exist.' },
+      ];
+
+      mockUpdateLoadBalancerConfigurationError(
+        loadbalancer.id,
+        configuration.id,
+        errors
+      ).as('updateConfigurationError');
+
+      cy.visitWithLogin(
+        `/loadbalancers/${loadbalancer.id}/configurations/${configuration.id}`
+      );
+
+      cy.wait([
+        '@getFeatureFlags',
+        '@getClientStream',
+        '@getLoadBalancer',
+        '@getConfigurations',
+      ]);
+
+      // In edit mode, we will disable the "save" button if the user hasn't made any changes
+      ui.button
+        .findByTitle('Save Configuration')
+        .should('be.visible')
+        .should('be.disabled');
+
+      cy.findByLabelText('Configuration Label')
+        .should('be.visible')
+        .clear()
+        .type('new-label');
+
+      ui.button
+        .findByTitle('Save Configuration')
+        .should('be.visible')
+        .should('be.enabled')
+        .click();
+
+      cy.wait('@updateConfigurationError');
+
+      for (const error of errors) {
+        cy.findByText(error.reason).should('be.visible');
+      }
+    });
+  });
+
   describe('delete', () => {
     it('deletes a configuration', () => {
       const loadbalancer = loadbalancerFactory.build();
diff --git a/packages/manager/cypress/support/intercepts/load-balancers.ts b/packages/manager/cypress/support/intercepts/load-balancers.ts
index 687240aea62..ff7ed60fbe2 100644
--- a/packages/manager/cypress/support/intercepts/load-balancers.ts
+++ b/packages/manager/cypress/support/intercepts/load-balancers.ts
@@ -119,6 +119,45 @@ export const mockCreateLoadBalancerConfiguration = (
   );
 };
 
+/**
+ * Intercepts PUT request to update an AGLB configuration.
+ *
+ * @param loadBalancerId - ID of load balancer for which to update the configuration.
+ * @param configuration - The AGLB configuration being updated.
+ *
+ * @returns Cypress chainable.
+ */
+export const mockUpdateLoadBalancerConfiguration = (
+  loadBalancerId: number,
+  configuration: Configuration
+) => {
+  return cy.intercept(
+    'PUT',
+    apiMatcher(`/aglb/${loadBalancerId}/configurations/${configuration.id}`),
+    makeResponse(configuration)
+  );
+};
+
+/**
+ * Intercepts PUT request to update an AGLB configuration.
+ *
+ * @param loadBalancerId - ID of load balancer for which to update the configuration.
+ * @param configuration - The AGLB configuration being updated.
+ *
+ * @returns Cypress chainable.
+ */
+export const mockUpdateLoadBalancerConfigurationError = (
+  loadBalancerId: number,
+  configurationId: number,
+  errors: APIError[]
+) => {
+  return cy.intercept(
+    'PUT',
+    apiMatcher(`/aglb/${loadBalancerId}/configurations/${configurationId}`),
+    makeResponse({ errors }, 400)
+  );
+};
+
 /**
  * Intercepts POST request to create an AGLB configuration and returns an error.
  *
diff --git a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Certificates/EditCertificateDrawer.test.tsx b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Certificates/EditCertificateDrawer.test.tsx
index 1bb38a1df5a..7efd1e5a9fa 100644
--- a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Certificates/EditCertificateDrawer.test.tsx
+++ b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Certificates/EditCertificateDrawer.test.tsx
@@ -1,4 +1,3 @@
-import { Certificate } from '@linode/api-v4';
 import { act, waitFor } from '@testing-library/react';
 import userEvent from '@testing-library/user-event';
 import React from 'react';
@@ -8,18 +7,19 @@ import { renderWithTheme } from 'src/utilities/testHelpers';
 
 import { EditCertificateDrawer } from './EditCertificateDrawer';
 
-const mockTLSCertificate: Certificate = {
+const mockTLSCertificate = {
   certificate: mockCertificate,
   id: 0,
   label: 'test-tls-cert',
   type: 'downstream',
-};
-const mockCACertificate: Certificate = {
+} as const;
+
+const mockCACertificate = {
   certificate: mockCertificate,
   id: 0,
   label: 'test-ca-cert',
   type: 'ca',
-};
+} as const;
 
 describe('EditCertificateDrawer', () => {
   it('should contain the name of the cert in the drawer title and label field', () => {
diff --git a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Certificates/EditCertificateDrawer.tsx b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Certificates/EditCertificateDrawer.tsx
index e9d20cfb6ab..9b9ca01ebe6 100644
--- a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Certificates/EditCertificateDrawer.tsx
+++ b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Certificates/EditCertificateDrawer.tsx
@@ -35,7 +35,7 @@ export const EditCertificateDrawer = (props: Props) => {
   const formik = useFormik<UpdateCertificatePayload>({
     enableReinitialize: true,
     initialValues: {
-      certificate: certificate?.certificate.trim(),
+      certificate: certificate?.certificate?.trim(),
       key: '',
       label: certificate?.label ?? '',
       type: certificate?.type,
@@ -43,7 +43,7 @@ export const EditCertificateDrawer = (props: Props) => {
     async onSubmit(values) {
       // The user has not edited their cert or the private key, so we exclude both cert and key from the request.
       const shouldIgnoreField =
-        certificate?.certificate.trim() === values.certificate &&
+        certificate?.certificate?.trim() === values.certificate &&
         values.key === '';
 
       try {
diff --git a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Configurations/ApplyCertificatesDrawer.tsx b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Configurations/ApplyCertificatesDrawer.tsx
index d6503b2b618..c823a573672 100644
--- a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Configurations/ApplyCertificatesDrawer.tsx
+++ b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Configurations/ApplyCertificatesDrawer.tsx
@@ -85,6 +85,7 @@ export const ApplyCertificatesDrawer = (props: Props) => {
                 )
               }
               errorText={formik.errors.certificates?.[index]?.['id']}
+              filter={{ type: 'downstream' }}
               loadbalancerId={loadbalancerId}
               value={id}
             />
diff --git a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Configurations/CertificateTable.tsx b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Configurations/CertificateTable.tsx
index 00154f2b99b..26822ecd702 100644
--- a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Configurations/CertificateTable.tsx
+++ b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Configurations/CertificateTable.tsx
@@ -8,18 +8,21 @@ import { TableCell } from 'src/components/TableCell';
 import { TableHead } from 'src/components/TableHead';
 import { TableRow } from 'src/components/TableRow';
 import { TableRowEmpty } from 'src/components/TableRowEmpty/TableRowEmpty';
+import { Typography } from 'src/components/Typography';
 import { useLoadBalancerCertificatesQuery } from 'src/queries/aglb/certificates';
 
-import type { Configuration } from '@linode/api-v4';
+import type { CertificateConfig, Configuration } from '@linode/api-v4';
+import type { FormikErrors } from 'formik';
 
 interface Props {
   certificates: Configuration['certificates'];
+  errors: FormikErrors<CertificateConfig>[] | string[];
   loadbalancerId: number;
   onRemove: (index: number) => void;
 }
 
 export const CertificateTable = (props: Props) => {
-  const { certificates, loadbalancerId, onRemove } = props;
+  const { certificates, errors, loadbalancerId, onRemove } = props;
 
   const { data } = useLoadBalancerCertificatesQuery(
     loadbalancerId,
@@ -40,10 +43,27 @@ export const CertificateTable = (props: Props) => {
         {certificates.length === 0 && <TableRowEmpty colSpan={3} />}
         {certificates.map((cert, idx) => {
           const certificate = data?.data.find((c) => c.id === cert.id);
+          const error = errors[idx];
+          const hostnameError =
+            typeof error !== 'string' ? error?.hostname : undefined;
+          const idError = typeof error !== 'string' ? error?.id : undefined;
+
+          const generalRowError = typeof error === 'string' ? error : idError;
+
           return (
             <TableRow key={idx}>
-              <TableCell>{certificate?.label ?? cert.id}</TableCell>
-              <TableCell>{cert.hostname}</TableCell>
+              <TableCell>
+                {certificate?.label ?? cert.id}
+                {generalRowError && (
+                  <Typography color="error">{generalRowError}</Typography>
+                )}
+              </TableCell>
+              <TableCell>
+                {cert.hostname}
+                {hostnameError && (
+                  <Typography color="error">{hostnameError}</Typography>
+                )}
+              </TableCell>
               <TableCell actionCell>
                 <IconButton
                   aria-label={`Remove Certificate ${
diff --git a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Configurations/ConfigurationForm.tsx b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Configurations/ConfigurationForm.tsx
index 353a22b2728..f197df4f51d 100644
--- a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Configurations/ConfigurationForm.tsx
+++ b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Configurations/ConfigurationForm.tsx
@@ -2,7 +2,7 @@ import {
   CreateConfigurationSchema,
   UpdateConfigurationSchema,
 } from '@linode/validation';
-import { useFormik } from 'formik';
+import { useFormik, yupToFormErrors } from 'formik';
 import React, { useMemo, useState } from 'react';
 import { useParams } from 'react-router-dom';
 
@@ -74,7 +74,7 @@ export const ConfigurationForm = (props: CreateProps | EditProps) => {
       ? useLoadBalancerConfigurationMutation
       : useLoadBalancerConfigurationCreateMutation;
 
-  const { error, isLoading, mutateAsync } = useMutation(
+  const { error, isLoading, mutateAsync, reset } = useMutation(
     loadbalancerId,
     configuration?.id ?? -1
   );
@@ -102,10 +102,24 @@ export const ConfigurationForm = (props: CreateProps | EditProps) => {
         helpers.setErrors(getFormikErrorsFromAPIErrors(error));
       }
     },
-    validationSchema,
+    validate(values) {
+      // We must use `validate` insted of validationSchema because Formik decided to convert
+      // "" to undefined before passing the values to yup. This makes it hard to validate `label`.
+      // See https://github.com/jaredpalmer/formik/issues/805
+      try {
+        validationSchema.validateSync(values, { abortEarly: false });
+        return {};
+      } catch (error) {
+        return yupToFormErrors(error);
+      }
+    },
+    // Prevent errors from being cleared when we show API errors
+    validateOnBlur: !error,
+    validateOnChange: !error,
   });
 
   const handleRemoveCert = (index: number) => {
+    formik.setFieldTouched('certificates');
     formik.values.certificates.splice(index, 1);
     formik.setFieldValue('certificates', formik.values.certificates);
   };
@@ -119,16 +133,22 @@ export const ConfigurationForm = (props: CreateProps | EditProps) => {
   };
 
   const handleAddCerts = (certificates: Configuration['certificates']) => {
+    formik.setFieldTouched('certificates');
     formik.setFieldValue('certificates', [
       ...formik.values.certificates,
       ...certificates,
     ]);
   };
 
+  const handleReset = () => {
+    formik.resetForm();
+    reset();
+  };
+
   const generalErrors = error?.reduce((acc, { field, reason }) => {
     if (
       !field ||
-      !['certificates', 'label', 'port', 'protocol'].includes(field)
+      (formik.values.protocol !== 'https' && field.startsWith('certificates'))
     ) {
       return acc ? `${acc}, ${reason}` : reason;
     }
@@ -197,6 +217,11 @@ export const ConfigurationForm = (props: CreateProps | EditProps) => {
                 />
               )}
             <CertificateTable
+              errors={
+                Array.isArray(formik.errors.certificates)
+                  ? formik.errors.certificates
+                  : []
+              }
               certificates={formik.values.certificates}
               loadbalancerId={loadbalancerId}
               onRemove={handleRemoveCert}
@@ -204,7 +229,6 @@ export const ConfigurationForm = (props: CreateProps | EditProps) => {
             <Box mt={2}>
               <Button
                 onClick={() => {
-                  formik.setFieldTouched('certificates');
                   setIsApplyCertDialogOpen(true);
                 }}
                 buttonType="outlined"
@@ -219,6 +243,9 @@ export const ConfigurationForm = (props: CreateProps | EditProps) => {
       <Divider spacingBottom={16} spacingTop={16} />
       <Stack spacing={2}>
         <Typography variant="h2">Routes</Typography>
+        {formik.errors.route_ids && (
+          <Notice text={formik.errors.route_ids} variant="error" />
+        )}
         <Stack direction="row" flexWrap="wrap" gap={2}>
           <Button
             buttonType="outlined"
@@ -241,15 +268,30 @@ export const ConfigurationForm = (props: CreateProps | EditProps) => {
       </Stack>
       <Divider spacingBottom={16} spacingTop={16} />
       <Stack direction="row" flexWrap="wrap" gap={2} justifyContent="flex-end">
+        {mode === 'edit' && formik.dirty && (
+          <Button buttonType="secondary" onClick={handleReset}>
+            Reset
+          </Button>
+        )}
+        {mode === 'edit' && (
+          <Button
+            buttonType="secondary"
+            onClick={() => setIsDeleteDialogOpen(true)}
+          >
+            Delete
+          </Button>
+        )}
+        {mode === 'create' && (
+          <Button buttonType="secondary" onClick={onCancel}>
+            Cancel
+          </Button>
+        )}
         <Button
-          onClick={
-            mode === 'edit' ? () => setIsDeleteDialogOpen(true) : onCancel
-          }
-          buttonType="secondary"
+          buttonType="primary"
+          disabled={mode === 'edit' && !formik.dirty}
+          loading={isLoading}
+          type="submit"
         >
-          {mode === 'edit' ? 'Delete' : 'Cancel'}
-        </Button>
-        <Button buttonType="primary" loading={isLoading} type="submit">
           {mode == 'edit' ? 'Save' : 'Create'} Configuration
         </Button>
       </Stack>
diff --git a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/LoadBalancerServiceTargets.tsx b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/LoadBalancerServiceTargets.tsx
index 1fbcec94796..c8b0e318bee 100644
--- a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/LoadBalancerServiceTargets.tsx
+++ b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/LoadBalancerServiceTargets.tsx
@@ -1,7 +1,7 @@
 import { ServiceTarget } from '@linode/api-v4';
 import CloseIcon from '@mui/icons-material/Close';
 import { Hidden, IconButton } from '@mui/material';
-import React, { useEffect, useState } from 'react';
+import React, { useState } from 'react';
 import { useParams } from 'react-router-dom';
 
 import { Button } from 'src/components/Button/Button';
@@ -66,13 +66,6 @@ export const LoadBalancerServiceTargets = () => {
     setSelectedServiceTarget(serviceTarget);
   };
 
-  // Once the drawer is closed, clear the selected service target for the correct add/edit drawer data.
-  useEffect(() => {
-    if (!isDrawerOpen) {
-      setSelectedServiceTarget(undefined);
-    }
-  }, [isDrawerOpen]);
-
   // If the user types in a search query, filter results by label.
   if (query) {
     filter['label'] = { '+contains': query };
@@ -148,10 +141,10 @@ export const LoadBalancerServiceTargets = () => {
             </TableSortCell>
             <Hidden smDown>
               <TableSortCell
-                active={orderBy === 'algorithm'}
+                active={orderBy === 'load_balancing_policy'}
                 direction={order}
                 handleClick={handleOrderChange}
-                label="algorithm"
+                label="load_balancing_policy"
               >
                 Algorithm
               </TableSortCell>
@@ -197,8 +190,11 @@ export const LoadBalancerServiceTargets = () => {
         pageSize={pagination.pageSize}
       />
       <ServiceTargetDrawer
+        onClose={() => {
+          setIsDrawerOpen(false);
+          setSelectedServiceTarget(undefined);
+        }}
         loadbalancerId={Number(loadbalancerId)}
-        onClose={() => setIsDrawerOpen(false)}
         open={isDrawerOpen}
         serviceTarget={selectedServiceTarget}
       />
diff --git a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Routes/RuleDrawer.tsx b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Routes/RuleDrawer.tsx
index dc77a6bafbc..680c9da69ff 100644
--- a/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Routes/RuleDrawer.tsx
+++ b/packages/manager/src/features/LoadBalancers/LoadBalancerDetail/Routes/RuleDrawer.tsx
@@ -89,6 +89,7 @@ export const RuleDrawer = (props: Props) => {
         }
 
         await updateRoute({
+          label: route?.label,
           protocol: route?.protocol,
           // If we are editing, send the updated rules, otherwise
           // append a new rule to the end.
diff --git a/packages/manager/src/queries/aglb/serviceTargets.ts b/packages/manager/src/queries/aglb/serviceTargets.ts
index c417d06a939..1dcc5560aa3 100644
--- a/packages/manager/src/queries/aglb/serviceTargets.ts
+++ b/packages/manager/src/queries/aglb/serviceTargets.ts
@@ -97,7 +97,7 @@ export const useLoadBalancerServiceTargetsInfiniteQuery = (
   filter: Filter = {}
 ) => {
   return useInfiniteQuery<ResourcePage<ServiceTarget>, APIError[]>(
-    [QUERY_KEY, 'loadbalancer', id, 'service-targets', 'infinite', filter],
+    [QUERY_KEY, 'aglb', id, 'service-targets', 'infinite', filter],
     ({ pageParam }) =>
       getLoadbalancerServiceTargets(
         id,
diff --git a/packages/validation/src/loadbalancers.schema.ts b/packages/validation/src/loadbalancers.schema.ts
index af4f3d80127..cd02d0b72bd 100644
--- a/packages/validation/src/loadbalancers.schema.ts
+++ b/packages/validation/src/loadbalancers.schema.ts
@@ -134,6 +134,7 @@ const BaseRuleSchema = object({
         return sum === 100;
       }
     )
+    .min(1, 'Rules must have at least 1 Service Target.')
     .required(),
 });