diff --git a/app/client/cypress/integration/Smoke_TestSuite/ClientSideTests/PropertyPane/PropertyPane_Search_spec.ts b/app/client/cypress/integration/Smoke_TestSuite/ClientSideTests/PropertyPane/PropertyPane_Search_spec.ts
index ac2a3ec8c3..515c126dfb 100644
--- a/app/client/cypress/integration/Smoke_TestSuite/ClientSideTests/PropertyPane/PropertyPane_Search_spec.ts
+++ b/app/client/cypress/integration/Smoke_TestSuite/ClientSideTests/PropertyPane/PropertyPane_Search_spec.ts
@@ -11,22 +11,34 @@ describe("Property Pane Search", function() {
     });
   });
 
-  // TODO(aswathkk): Fix /ClientSideTests/IDE/Canvas_Context_Property_Pane_spec.js and uncomment this
-  // it("1. Verify if the search Input is getting focused when a widget is selected", function() {
-  //   ee.SelectEntityByName("Table1", "Widgets");
+  it("1. Verify if the search Input is getting focused when a widget is selected", function() {
+    ee.SelectEntityByName("Table1", "Widgets");
 
-  //   // Initially the search input will only be soft focused
-  //   // We need to press Enter to properly focus it
-  //   agHelper.PressEnter();
-  //   agHelper.AssertElementFocus(propPane._propertyPaneSearchInput);
+    // Initially the search input will only be soft focused
+    // We need to press Enter to properly focus it
+    agHelper.AssertElementFocus(propPane._propertyPaneSearchInputWrapper);
+    agHelper.PressEnter();
+    agHelper.AssertElementFocus(propPane._propertyPaneSearchInput);
 
-  //   // Pressing Escape should soft focus the search input
-  //   agHelper.PressEscape();
-  //   agHelper.AssertElementFocus(propPane._propertyPaneSearchInput, false);
-  // });
+    // Pressing Escape should soft focus the search input
+    agHelper.PressEscape();
+    agHelper.AssertElementFocus(propPane._propertyPaneSearchInputWrapper);
+
+    // Opening a panel should focus the search input
+    propPane.OpenTableColumnSettings("name");
+    agHelper.AssertElementFocus(propPane._propertyPaneSearchInputWrapper);
+
+    // Opening some other widget and then going back to the initial widget should soft focus the search input that is inside a panel
+    ee.SelectEntityByName("Switch1", "Widgets");
+    ee.SelectEntityByName("Table1", "Widgets");
+    agHelper.AssertElementFocus(propPane._propertyPaneSearchInputWrapper);
+
+    // Going out of the panel should soft focus the search input
+    propPane.NavigateBackToPropertyPane();
+    agHelper.AssertElementFocus(propPane._propertyPaneSearchInputWrapper);
+  });
 
   it("2. Search for Properties", function() {
-    ee.SelectEntityByName("Table1", "Widgets");
     // Search for a property inside content tab
     propPane.Search("visible");
     propPane.AssertIfPropertyOrSectionExists("general", "CONTENT", "visible");
diff --git a/app/client/cypress/support/Pages/PropertyPane.ts b/app/client/cypress/support/Pages/PropertyPane.ts
index 099c969e29..19e8737764 100644
--- a/app/client/cypress/support/Pages/PropertyPane.ts
+++ b/app/client/cypress/support/Pages/PropertyPane.ts
@@ -46,7 +46,8 @@ export class PropertyPane {
     `.t--property-pane-section-collapse-${section} .t--property-section-tag-${tab}`;
   private _propertyControl = (property: string) =>
     `.t--property-control-${property}`;
-  _propertyPaneSearchInput = ".t--property-pane-search-input-wrapper input";
+  _propertyPaneSearchInputWrapper = ".t--property-pane-search-input-wrapper";
+  _propertyPaneSearchInput = `${this._propertyPaneSearchInputWrapper} input`;
   _propertyPaneEmptySearchResult = ".t--property-pane-no-search-results";
   _propertyToggle = (controlToToggle: string) =>
     ".t--property-control-" +
diff --git a/app/client/src/pages/Editor/PropertyPane/PropertyPaneSearchInput.tsx b/app/client/src/pages/Editor/PropertyPane/PropertyPaneSearchInput.tsx
index 0a9ccf12d4..86a98c772c 100644
--- a/app/client/src/pages/Editor/PropertyPane/PropertyPaneSearchInput.tsx
+++ b/app/client/src/pages/Editor/PropertyPane/PropertyPaneSearchInput.tsx
@@ -3,12 +3,12 @@ import styled from "styled-components";
 import { SearchVariant } from "design-system";
 import { InputWrapper, SearchInput } from "design-system";
 import { Colors } from "constants/Colors";
-// import { useSelector } from "react-redux";
-// import {
-//   getShouldFocusPanelPropertySearch,
-//   getShouldFocusPropertySearch,
-// } from "selectors/propertyPaneSelectors";
-// import { isCurrentFocusOnInput } from "utils/editorContextUtils";
+import { useSelector } from "react-redux";
+import {
+  getShouldFocusPanelPropertySearch,
+  getShouldFocusPropertySearch,
+} from "selectors/propertyPaneSelectors";
+import { isCurrentFocusOnInput } from "utils/editorContextUtils";
 import { PROPERTY_SEARCH_INPUT_PLACEHOLDER } from "@appsmith/constants/messages";
 
 const SearchInputWrapper = styled.div`
@@ -37,28 +37,30 @@ type PropertyPaneSearchInputProps = {
 export function PropertyPaneSearchInput(props: PropertyPaneSearchInputProps) {
   const wrapperRef = useRef<HTMLDivElement>(null);
   const inputRef = useRef<HTMLDivElement>(null);
+  const shouldFocusSearch = useSelector(getShouldFocusPropertySearch);
+  const shouldFocusPanelSearch = useSelector(getShouldFocusPanelPropertySearch);
+  const isPanel = !!props.isPanel;
 
-  // TODO(aswathkk): Fix /ClientSideTests/IDE/Canvas_Context_Property_Pane_spec.js and uncomment this
-  // const shouldFocusSearch = useSelector(getShouldFocusPropertySearch);
-  // const shouldFocusPanelSearch = useSelector(getShouldFocusPanelPropertySearch);
-
-  // useEffect(() => {
-  //   // Checks if the property pane opened not because of focusing an input inside a widget
-  //   // The same functionality is being used for context preservation. Need to check if we can piggy back on that.
-  //   const isActiveFocusNotFromWidgetInput = !isCurrentFocusOnInput();
-  //   if (shouldFocusSearch && isActiveFocusNotFromWidgetInput) {
-  //     if (!props.isPanel && !shouldFocusPanelSearch) {
-  //       setTimeout(() => {
-  //         wrapperRef.current?.focus();
-  //       });
-  //     } else if (props.isPanel && shouldFocusPanelSearch) {
-  //       // Layered panels like Column Panel's transition takes 300ms
-  //       setTimeout(() => {
-  //         wrapperRef.current?.focus();
-  //       }, 300);
-  //     }
-  //   }
-  // }, [shouldFocusSearch, shouldFocusPanelSearch, props.isPanel]);
+  useEffect(() => {
+    // Checks if the property pane opened not because of focusing an input inside a widget
+    const isActiveFocusNotFromWidgetInput = !isCurrentFocusOnInput();
+    if (
+      shouldFocusSearch &&
+      isActiveFocusNotFromWidgetInput &&
+      // while the panel transition happens, focus will be happening twice. Once on the main pane and then on the panel
+      // The following check will make sure that the focus is only done once and prevents the UI jittering
+      isPanel === shouldFocusPanelSearch
+    ) {
+      setTimeout(
+        () => {
+          wrapperRef.current?.focus();
+        },
+        // Layered panels like Column Panel's transition takes 300ms.
+        // To avoid UI jittering, we are delaying the focus by 300ms.
+        isPanel ? 300 : 0,
+      );
+    }
+  }, [shouldFocusSearch, shouldFocusPanelSearch, isPanel]);
 
   const handleInputKeydown = useCallback((e: KeyboardEvent) => {
     switch (e.key) {