diff --git a/ui/apps/platform/src/Containers/Collections/CollectionForm.tsx b/ui/apps/platform/src/Containers/Collections/CollectionForm.tsx
index ad29907d4ef30..30bcd603e387f 100644
--- a/ui/apps/platform/src/Containers/Collections/CollectionForm.tsx
+++ b/ui/apps/platform/src/Containers/Collections/CollectionForm.tsx
@@ -212,6 +212,7 @@ function CollectionForm({
                         </>
                     )}
                     <RuleSelector
+                        collection={values}
                         entityType="Deployment"
                         scopedResourceSelector={values.resourceSelector.Deployment}
                         handleChange={onResourceSelectorChange}
@@ -222,6 +223,7 @@ function CollectionForm({
                         in
                     </Label>
                     <RuleSelector
+                        collection={values}
                         entityType="Namespace"
                         scopedResourceSelector={values.resourceSelector.Namespace}
                         handleChange={onResourceSelectorChange}
@@ -232,6 +234,7 @@ function CollectionForm({
                         in
                     </Label>
                     <RuleSelector
+                        collection={values}
                         entityType="Cluster"
                         scopedResourceSelector={values.resourceSelector.Cluster}
                         handleChange={onResourceSelectorChange}
diff --git a/ui/apps/platform/src/Containers/Collections/RuleSelector/AutoCompleteSelect.tsx b/ui/apps/platform/src/Containers/Collections/RuleSelector/AutoCompleteSelect.tsx
index a5289d4f4af65..3da664f063aea 100644
--- a/ui/apps/platform/src/Containers/Collections/RuleSelector/AutoCompleteSelect.tsx
+++ b/ui/apps/platform/src/Containers/Collections/RuleSelector/AutoCompleteSelect.tsx
@@ -1,6 +1,8 @@
-import React from 'react';
-import { Select, ValidatedOptions } from '@patternfly/react-core';
+import React, { ReactElement, ReactNode, useCallback, useMemo, useState } from 'react';
+import { debounce, Select, SelectOption, ValidatedOptions } from '@patternfly/react-core';
 import useSelectToggle from 'hooks/patternfly/useSelectToggle';
+import useRestQuery from 'Containers/Dashboard/hooks/useRestQuery';
+import { CancellableRequest } from 'services/cancellationUtils';
 
 export type AutoCompleteSelectProps = {
     id: string;
@@ -10,9 +12,19 @@ export type AutoCompleteSelectProps = {
     onChange: (value: string) => void;
     validated: ValidatedOptions;
     isDisabled: boolean;
+    autocompleteProvider?: (search: string) => CancellableRequest<string[]>;
+    OptionComponent?: ReactNode;
 };
 
-/* TODO Implement autocompletion */
+function getOptions(
+    OptionComponent: ReactNode,
+    data: string[] | undefined
+): ReactElement[] | undefined {
+    return data?.map((value) => (
+        <SelectOption key={value} value={value} component={OptionComponent} />
+    ));
+}
+
 export function AutoCompleteSelect({
     id,
     selectedOption,
@@ -21,14 +33,36 @@ export function AutoCompleteSelect({
     onChange,
     validated,
     isDisabled,
+    autocompleteProvider,
+    OptionComponent = SelectOption,
 }: AutoCompleteSelectProps) {
     const { isOpen, onToggle, closeSelect } = useSelectToggle();
+    const [typeahead, setTypeahead] = useState(selectedOption);
+
+    const autocompleteCallback = useCallback(() => {
+        const shouldMakeRequest = isOpen && autocompleteProvider;
+        if (shouldMakeRequest) {
+            return autocompleteProvider(typeahead);
+        }
+        return {
+            request: Promise.resolve([]),
+            cancel: () => {},
+        };
+    }, [isOpen, autocompleteProvider, typeahead]);
+
+    const { data } = useRestQuery(autocompleteCallback);
 
     function onSelect(_, value) {
         onChange(value);
         closeSelect();
     }
 
+    // Debounce the autocomplete requests to not overload the backend
+    const updateTypeahead = useMemo(
+        () => debounce((value: string) => setTypeahead(value), 800),
+        []
+    );
+
     return (
         <>
             <Select
@@ -39,11 +73,15 @@ export function AutoCompleteSelect({
                 variant="typeahead"
                 isCreatable
                 isOpen={isOpen}
+                onFilter={() => getOptions(OptionComponent, data)}
                 onToggle={onToggle}
+                onTypeaheadInputChanged={updateTypeahead}
                 selections={selectedOption}
                 onSelect={onSelect}
                 isDisabled={isDisabled}
-            />
+            >
+                {getOptions(OptionComponent, data)}
+            </Select>
         </>
     );
 }
diff --git a/ui/apps/platform/src/Containers/Collections/RuleSelector/ByLabelSelector.tsx b/ui/apps/platform/src/Containers/Collections/RuleSelector/ByLabelSelector.tsx
index 2b48f3f642954..34708cc8ed6ef 100644
--- a/ui/apps/platform/src/Containers/Collections/RuleSelector/ByLabelSelector.tsx
+++ b/ui/apps/platform/src/Containers/Collections/RuleSelector/ByLabelSelector.tsx
@@ -201,6 +201,7 @@ function ByLabelSelector({
                                                         }
                                                     >
                                                         <TrashIcon
+                                                            aria-label={`Delete ${value}`}
                                                             style={{ cursor: 'pointer' }}
                                                             color="var(--pf-global--Color--dark-200)"
                                                         />
diff --git a/ui/apps/platform/src/Containers/Collections/RuleSelector/ByNameSelector.tsx b/ui/apps/platform/src/Containers/Collections/RuleSelector/ByNameSelector.tsx
index 35704fb6cbecb..2eb14a170d5aa 100644
--- a/ui/apps/platform/src/Containers/Collections/RuleSelector/ByNameSelector.tsx
+++ b/ui/apps/platform/src/Containers/Collections/RuleSelector/ByNameSelector.tsx
@@ -1,14 +1,22 @@
-import React from 'react';
+import React, { ReactNode, useCallback } from 'react';
 import { Button, Flex, FormGroup, ValidatedOptions } from '@patternfly/react-core';
 import { TrashIcon } from '@patternfly/react-icons';
 import cloneDeep from 'lodash/cloneDeep';
 
 import { FormikErrors } from 'formik';
 import useIndexKey from 'hooks/useIndexKey';
+import { getCollectionAutoComplete } from 'services/CollectionsService';
 import { AutoCompleteSelect } from './AutoCompleteSelect';
-import { ByNameResourceSelector, ScopedResourceSelector, SelectorEntityType } from '../types';
+import {
+    ByNameResourceSelector,
+    Collection,
+    ScopedResourceSelector,
+    SelectorEntityType,
+} from '../types';
+import { generateRequest } from '../converter';
 
 export type ByNameSelectorProps = {
+    collection: Collection;
     entityType: SelectorEntityType;
     scopedResourceSelector: ByNameResourceSelector;
     handleChange: (
@@ -17,16 +25,26 @@ export type ByNameSelectorProps = {
     ) => void;
     validationErrors: FormikErrors<ByNameResourceSelector> | undefined;
     isDisabled: boolean;
+    OptionComponent: ReactNode;
 };
 
 function ByNameSelector({
+    collection,
     entityType,
     scopedResourceSelector,
     handleChange,
     validationErrors,
     isDisabled,
+    OptionComponent,
 }: ByNameSelectorProps) {
     const { keyFor, invalidateIndexKeys } = useIndexKey();
+    const autocompleteProvider = useCallback(
+        (search: string) => {
+            const req = generateRequest(collection);
+            return getCollectionAutoComplete(req.resourceSelectors, entityType, search);
+        },
+        [collection, entityType]
+    );
 
     function onAddValue() {
         const selector = cloneDeep(scopedResourceSelector);
@@ -77,6 +95,8 @@ function ByNameSelector({
                                     : ValidatedOptions.default
                             }
                             isDisabled={isDisabled}
+                            autocompleteProvider={autocompleteProvider}
+                            OptionComponent={OptionComponent}
                         />
                         {!isDisabled && (
                             <Button variant="plain" onClick={() => onDeleteValue(index)}>
diff --git a/ui/apps/platform/src/Containers/Collections/RuleSelector/RuleSelector.test.tsx b/ui/apps/platform/src/Containers/Collections/RuleSelector/RuleSelector.test.tsx
index 7246aa1c78373..e1bf0ffbccac9 100644
--- a/ui/apps/platform/src/Containers/Collections/RuleSelector/RuleSelector.test.tsx
+++ b/ui/apps/platform/src/Containers/Collections/RuleSelector/RuleSelector.test.tsx
@@ -3,9 +3,17 @@ import { render, screen } from '@testing-library/react';
 import userEvent from '@testing-library/user-event';
 import '@testing-library/jest-dom/extend-expect';
 
+import { mockDebounce } from 'test-utils/mocks/@patternfly/react-core';
 import RuleSelector from './RuleSelector';
 import { ByLabelResourceSelector, ByNameResourceSelector, ScopedResourceSelector } from '../types';
 
+jest.mock('@patternfly/react-core', () => mockDebounce);
+
+jest.mock('services/CollectionsService', () => ({
+    __esModule: true,
+    getCollectionAutoComplete: () => ({ request: Promise.resolve([]) }),
+}));
+
 // Component wrapper to allow a higher level component to feed updated state back to the RuleSelector.
 function DeploymentRuleSelector({ defaultSelector, onChange }) {
     const [resourceSelector, setResourceSelector] =
@@ -17,6 +25,17 @@ function DeploymentRuleSelector({ defaultSelector, onChange }) {
 
     return (
         <RuleSelector
+            collection={{
+                name: '',
+                description: '',
+                inUse: false,
+                resourceSelector: {
+                    Deployment: { type: 'All' },
+                    Namespace: { type: 'All' },
+                    Cluster: { type: 'All' },
+                },
+                embeddedCollectionIds: [],
+            }}
             entityType="Deployment"
             scopedResourceSelector={resourceSelector}
             handleChange={(_, newSelector) => setResourceSelector(newSelector)}
@@ -168,19 +187,14 @@ describe('Collection RuleSelector component', () => {
         );
         await user.type(
             screen.getByLabelText('Select label value 1 of 1 for deployment rule 2 of 2'),
-            // typo
-            'stabl{Enter}'
+            'stable{Enter}'
         );
+
         await user.click(screen.getAllByText('Add value')[1]);
         await user.type(
             screen.getByLabelText('Select label value 2 of 2 for deployment rule 2 of 2'),
             'beta{Enter}'
         );
-        // test editing typo
-        await user.type(
-            screen.getByLabelText('Select label value 1 of 2 for deployment rule 2 of 2'),
-            'e{Enter}'
-        );
 
         expect(resourceSelector).toEqual({
             type: 'ByLabel',
@@ -198,5 +212,15 @@ describe('Collection RuleSelector component', () => {
                 },
             ],
         });
+
+        // Check that deletion of all items removes the selector
+        await user.click(screen.getByLabelText('Delete stable'));
+        await user.click(screen.getByLabelText('Delete beta'));
+        await user.click(screen.getByLabelText('Delete visa-processor'));
+        await user.click(screen.getByLabelText('Delete mastercard-processor'));
+        await user.click(screen.getByLabelText('Delete discover-processor'));
+
+        expect(resourceSelector).toEqual({ type: 'All' });
+        expect(screen.getByText('All deployments')).toBeInTheDocument();
     });
 });
diff --git a/ui/apps/platform/src/Containers/Collections/RuleSelector/RuleSelector.tsx b/ui/apps/platform/src/Containers/Collections/RuleSelector/RuleSelector.tsx
index 16282cb75e615..2c795b5bcecb0 100644
--- a/ui/apps/platform/src/Containers/Collections/RuleSelector/RuleSelector.tsx
+++ b/ui/apps/platform/src/Containers/Collections/RuleSelector/RuleSelector.tsx
@@ -1,10 +1,12 @@
-import React from 'react';
+import React, { ForwardedRef, forwardRef, ReactNode } from 'react';
 import { Select, SelectOption } from '@patternfly/react-core';
 import pluralize from 'pluralize';
 import { FormikErrors } from 'formik';
 
 import useSelectToggle from 'hooks/patternfly/useSelectToggle';
+import ResourceIcon from 'Components/PatternFly/ResourceIcon';
 import {
+    Collection,
     RuleSelectorOption,
     ScopedResourceSelector,
     SelectorEntityType,
@@ -18,6 +20,7 @@ function isRuleSelectorOption(value: string): value is RuleSelectorOption {
 }
 
 export type RuleSelectorProps = {
+    collection: Collection;
     entityType: SelectorEntityType;
     scopedResourceSelector: ScopedResourceSelector;
     handleChange: (
@@ -29,6 +32,7 @@ export type RuleSelectorProps = {
 };
 
 function RuleSelector({
+    collection,
     entityType,
     scopedResourceSelector,
     handleChange,
@@ -38,6 +42,20 @@ function RuleSelector({
     const { isOpen, onToggle, closeSelect } = useSelectToggle();
     const pluralEntity = pluralize(entityType);
 
+    // We need to wrap this custom SelectOption component in a forward ref
+    // because PatternFly will pass a `ref` to it
+    const OptionComponent = forwardRef(
+        (
+            props: { className: string; children: ReactNode },
+            ref: ForwardedRef<HTMLButtonElement | null>
+        ) => (
+            <button className={props.className} type="button" ref={ref}>
+                <ResourceIcon kind={entityType} />
+                {props.children}
+            </button>
+        )
+    );
+
     function onRuleOptionSelect(_, value) {
         if (!isRuleSelectorOption(value)) {
             return;
@@ -84,11 +102,13 @@ function RuleSelector({
 
             {scopedResourceSelector.type === 'ByName' && (
                 <ByNameSelector
+                    collection={collection}
                     entityType={entityType}
                     scopedResourceSelector={scopedResourceSelector}
                     handleChange={handleChange}
                     validationErrors={validationErrors}
                     isDisabled={isDisabled}
+                    OptionComponent={OptionComponent}
                 />
             )}
 
diff --git a/ui/apps/platform/src/Containers/Dashboard/hooks/useRestQuery.ts b/ui/apps/platform/src/Containers/Dashboard/hooks/useRestQuery.ts
index 894ea98134a32..efc3f06c09e1e 100644
--- a/ui/apps/platform/src/Containers/Dashboard/hooks/useRestQuery.ts
+++ b/ui/apps/platform/src/Containers/Dashboard/hooks/useRestQuery.ts
@@ -19,6 +19,7 @@ export default function useRestQuery<ReturnType>(
         const { request, cancel } = cancellableRequestFn();
 
         setError(undefined);
+        setLoading(true);
 
         request
             .then((result) => {
diff --git a/ui/apps/platform/src/services/CollectionsService.ts b/ui/apps/platform/src/services/CollectionsService.ts
index 2c783991d3ca0..761f02dca94eb 100644
--- a/ui/apps/platform/src/services/CollectionsService.ts
+++ b/ui/apps/platform/src/services/CollectionsService.ts
@@ -211,13 +211,13 @@ export function getCollectionAutoComplete(
     searchCategory: string,
     searchLabel: string
 ): CancellableRequest<string[]> {
-    const params = qs.stringify(
-        { resourceSelectors, searchCategory, searchLabel },
-        { arrayFormat: 'repeat' }
-    );
     return makeCancellableAxiosRequest((signal) =>
         axios
-            .get<{ values: string[] }>(`${collectionsAutocompleteUrl}?${params}`, { signal })
+            .post<{ values: string[] }>(
+                collectionsAutocompleteUrl,
+                { resourceSelectors, searchCategory, searchLabel },
+                { signal }
+            )
             .then((response) => response.data.values)
     );
 }
diff --git a/ui/apps/platform/src/test-utils/mocks/@patternfly/react-core.tsx b/ui/apps/platform/src/test-utils/mocks/@patternfly/react-core.tsx
new file mode 100644
index 0000000000000..05cd2c19c57da
--- /dev/null
+++ b/ui/apps/platform/src/test-utils/mocks/@patternfly/react-core.tsx
@@ -0,0 +1,9 @@
+import * as PFReactCore from '@patternfly/react-core';
+
+const { debounce, ...rest } = jest.requireActual('@patternfly/react-core');
+
+// Overrides the PF `debounce` function to do nothing other than return the original function. This
+// can be used to avoid issues in tests that result from state updates in a debounced function.
+export const mockDebounce = { ...rest, debounce: (fn: () => void) => fn } as jest.Mock<
+    typeof PFReactCore
+>;